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FORAGING AND REPRODUCTIVE ECOLOGY IN A COMMUNITY 
OF BATS IN PANAMA 



By 



FRANK JOSEPH BONACCORSO 



A DISSERTATION PRESENTED TO THE GRADUATE COUNCIL OF 
THE UNIVERSITY OF FLORIDA IN PARTIAL 
FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF 
DOCTOR OF PHILOSOPHY 



UNIVERSITY OF FLORIDA 
1975 



This work is dedicated to Clark Sanford, Julie Wiatt, and Bill 
Blven, my field assistants, who endured a year of damp weather, irritat- 
ing insects, bat bites, tough pork chops, and numerous other tropical 
hardships, yet shared the enumerable joys we encountered. We learned 
much together of tropical forests and ourselves and are better people 
f o r it, 



ACKNOWLEDGMENTS 

This study was funded by NSF Grant GB-3&068 to Dr, J. H. Kaufmann, 
NIH Biomedical Sciences Grant No. RR7021-07 from the Division of Spon- 
sored Research of the University of Florida to Dr, S, R. Humphrey, and 
the Environmental Sciences Program of the Smithsonian Tropical Research 
Institute. The Florida State Museum and Smithsonian Tropical Research 
Institute provided logistical support. 

Dr. B. K, McNab, both in his writings and classroom discussions, 
induced and encouraged the "germplasm" of interest which launched me 
into the study of the ecology of tropical bat communities. Drs. S. R. 
Humphrey, J, H. Kaufmann, E, Leigh, N. Smythe, A. F. Carr, D. H. Hirth, 
and T, C, Lmmel unselfishly took time to provide constructive guidance. 
Dr, Robin Foster verified my seed identifications and cultured in me a 
deep appreciation for tropical plant ecology, Clark Sandford, Julie 
Wiatt, Bill Biven, and Janet Hall faithfully assisted with fieldwork and 
laboratory preparations under trying conditions. The creative talents 
of Nancy Halliday and Sylvia Scudder have rendered the illustrations. 
Finally, i wish to thank the scientists, students, and visitors 
coinciding with my residence on BCI, as well as the Smithsonian staff, 
for bringing encouragement, friendship, intellectual atmosphere, and 
volleyball to an isolate field station and making 1973 the most pleasant 
and memorable year I have experienced. 

i i i 



TABLE OF CONTENTS 

Page 

AKNOWLEDGEMENTS i I i 

ABSTRACT v 

INTRODUCTION 1 

STUDY AREA 3 

MATERIALS AND METHODS 6 

Mathematics 1 Formulae 10 

PHENOLOGY AND FOOD RESOURCES 12 

SPECIES DIVERSITY.. 20 

RESOURCE PARTITIONING 27 

Canopy Frugivore Guild 31 

Groundstory Frugivore Guild 50 

Scavenging Frugivore Guild 62 

Nectar-Pollen-Fruit-Insect Omnivore Guild 65 

Sangu i vore Guild 70 

Gleaning Carnivore Guild..... 73 

Slow-Flying Hawking Insectivore Guild 80 

REPRODUCTION 87 

Canopy Frugivore Guild •- 87 

Groundstory Frugivore. Guild - 9^ 

.Scavenging Frugivore Guild 97 

Nectar-Pollen-Fruit-Insect Omnivore Guild 97 

Sangu i vore Guild...... 97 

Gleaning Carnivore Guild 97 

Slow-Flying Hawking Insectivore Guild 98 

CONCLUSIONS , - 101 

Species Diversity And Phenology , 1 01 

Foraging And Reproductive Strategies 10^+ 

LITERATURE CITED 115 

APPENDIX 120 

B I 0GRAPH I CAL SKETCH 122 

iv 



Abstract of Dissertation Presented to the 
Graduate Council of the University of Florida in Partial 
Fulfillment of the Requirements for the Degree of Doctor of Philosophy 



FORAGING AND REPRODUCTIVE ECOLOGY IN A COMMUNITY 
OF BATS IN PANAMA 



By 
Frank Joseph Bonaccorso 
August, 1975 

Chairman: Dr. John H. Kaufmann 
Major Department: Zoology 

Resource partitioning, reproduction, species diversity, and 
community structure in a forest community of 35 bat species were 
studfed on Berro Colorado Island, Panama Canal Zone. Sixteen months 
of field-work were conducted between July 1971 and August 197^. Over 
2,800 bats Were captured, banded, and released with data collected on 
food habits, activity cycles, habitat selection, reproductive timing, 
and morphological feeding adaptations for each species. Information on 
the seasonality and abundance of fruit, flower, and insect resources 
used by bats also was collected. 

The diversity of tropical lowland bat communities in any one 
habitat changes significantly on a seasonal basis. Fluctuating levels 
of food resources require that many species utilize different habitats 
and foraging strategies through a year. Competitive interactions, 
predator avoidance, and climatic fluctuation further influence the 

v 



foraging strategies of each species. Tropical bat faunas can be 
broken down into feeding guilds on the basis of general food habits 
and method of food procurement. Within the most complex guilds, such 
as the canopy frugivore guild, food resources are partitioned in time 
and space and by size and quality. Within the simplest guilds food 
resources are partitioned primarily by food particle size. The most 
important mechanism of resource partitioning separating similar species 
is food particle size. Some species complexes appear to be limited not by 
absolute amount of food but by the distribution of those resources in 
a few concentrated patches accessible, to only a limited number of 
individuals at a given time. Reproduction coincides with high levels 
of available food resources within each feeding guild. 



V ! 



INTRODUCTION 

Mention of the words "tropical forest" among ecologists typically 
triggers visions of species rich communities, complex competitive inter- 
actions, and relatively stable environmental conditions. Indeed, fauna! 
lists in the tropics are large, and food webs are intricately complex. 
It is also true that organisms inhabiting tropical latitudes usually are 
subjected to less extreme environmental fluctuations than are their 
counterparts in temperate or polar regions. However, it is too infre- 
quently emphasized that even species in tropical forests must possess 
behavioral flexibility to counter and survive climatic and biotic 
environmental change. There are two major reasons for this general lack 
of insight. Firstly, few detailed studies of tropical organisms have 
spanned periods of several years or even seasons. And secondly, the 
behavioral responses of tropical species to environmental fluctuations 
are often quite subtle. Whereas temperate animals commonly exhibit 
obvious and dramatic reactions to seasonal change such as hibernation 
or long distance migration, tropical species may only need to switch 
food types or microhabi tats , or briefly halt reproduction. Nevertheless, 
genetic and behavioral flexibility are requisites for survival for most 
tropical as well as temperate species. 

Tropical bats are particularly worthwhile subjects for studies of 
diversity, competitive interaction, and response to environmental fluc- 
tuation because of their individual abundance and the complex taxonomic 

1 



2 

and ecological communities they form. About 100 species of bats occur 
in each of the small countries of Central America (Hall and Kelson, 
1959). It is common to find 30 to 50 species in one macrohabitat measur- 
ing a few square kilometers in area. For example Barro Colorado Island 
(15 sq km), Panama, currently supports populations of at least 35 species. 

Among tropical bat species, few ere known or suspected to reproduce 
year round or to specialize on constantly abundant food resources. The 
common vampire bat, Desmodus rot undus , is one notable exception (Wimsatt 
and Trapido, 1952). Instead, most bats, even in equatorial regions, are 
seasonally polyestrous or manes trous in reproduction (Baker and Baker, 
1936; Mutere, 1970; Fleming, 1373) and make seasonal shifts in food 
habits (Wilson, 1971b; Fleming et_ aj_. , 1972; He I thaus e£ aiL , 1975). 

The objective of this dissertation is to delineate adaptive strate- 
gies used by tropical bats that enable them to survive fluctuating 
environmental conditions and coexist with numerous similar species in 
complex communities. The field work represented herein documents 
seasonal changes in diversity, mechanisms of resource partitioning, and 
reproductive timing through one complete year and portions of two other 
years.. , 



STUDY AREA 
The primary research site was on Barro Colorado Island (BCI). 

Barro Colorado lies within freshwater Lake Gatun, in the Panama Canal 

o ' 

Zone, at 9 10 North latitude and 79° 51 ' West longitude. This field 

site was selected because it has a rich bat fauna, relatively undis- 
turbed mature moist forest, modern living and laboratory facilities, 
and reference collections of animals and plants. A secondary site was 
located on the mainland opposite BCI at the base of Buena Vista Penin- 
sula. 

The climate of this lowland area of Panama is warm and humid with 
a seven-month wet season and a three-month dry season. Dry season 
months, January through March, each receive less than 60 mm of rain. 
Wef season months, May through November, typically receive in excess 
of 250 .mm of rain. April and December are months of transition between 
dry and wet seasons and receive amounts of rain that vary considerably 
from year to year. Thus in years when April and December are very dry, 
the dry season may last for five months. Average annual rainfall since 
1926 has been 2,820 mm (Smythe, 1974). Monthly sums of rainfall for 
1973 are shown in Table 1. 

During night time sampling of bats, relative humidity under the 
forest canopy never fell below 80 percent. Measurements were made at 
2 m above ground with a sling pyschrometer . Daily temperatures on the 
forest floor fluctuate from a mean minimum of 22.1° C to a mean maximum 
of 28.0 C with no significant seasonal variation (Smythe, 197^). 



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Barro Colorado is in the Iropical Moist Forest life zone (Holdridge, 
I967). This 15 km island is covered with mature forest that is over 
60 years in age. The only human disturbance to the vegetation results 
from re-cutting forest trails and maintaining a small laboratory clear- 
ing, and an undetermined amount of illegal poaching. Further details 
on the geology, climate, biology, and history of the island are given by 
Kaufrnann (19&2) and Foster (1973). 



MATERIALS AND METHODS 

Seventeen sampling stations were located in an approximately 2 km 
central strip of Barro Colorado Island and one station was on Buena Vista 
Peninsula (Fig. 1). Habitats sampled during the study are classified as 
mature forest (]h stations on BCI), creeks (3 stations on BCI), and 
second growth (1 station on Buena Vista). The mature forest has a com- 
pletely closed canopy and is a minimum of 60 years old in all places. 
Some tracts within the forest have been undisturbed for 400 years 
(Robin Foster, pers. comm.). The creek stations are lined with rich 
shrub growth and the creek bed receives direct sunlight. The second 
growth habitat at Buena Vista is approximately 20 years old and consists 
of thick shrub growth and scattered small trees that form a discontin- 
uous canopy. 

Except on rare occasions when nets were damaged by tree falls or 
vandalized by poachers, each sampling station consisted of four or six 
6 x 2 m mist nets and one or two Tuttle harp traps (described in Tuttle, 
197*0 set across permanent trails. Nets were set in pairs at 100 m 
intervals, with one of each pair at ground level (0 to 3 m) and the other 
at subcanopy and lower canopy level (3 to 12 m) . Early in the study nets 
were rigged in the canopy as high as 25 m above ground, but use of these 
nets was soon discontinued because few bats were captured in them, which 
seemed to reflect a lack of much flight activity in the canopy levels. 
Harp traps were usually set at ground level in low, narrow tunnel-like 
passages created by the vegetation and trails. At a few stations where 



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the vegetation permitted, harp traps were rigged in subcanopy level 
"tunnel s". 

Nets and traps were open from sunset to sunrise 67 times between 
11 January and 31 December 19/3- On 28 other nights during that period 
sampling was conducted for less than a full night. The total sampling 
during 1973 involved 4,376 net-hours, 1,213 trap-hours, and 2,324 
captured bats. 

In 1971, 3^7 net"hours of sampling during a pilot study yielded 
282 bats between 20 June and 18 August. In 1974, 454 net-hours of 
additional sampling yielded 278 bats between 10 June and 17 July. No 
harp traps were available during these times for effective sampling of 
small insectivorous bats. 

Because Crespo e_t_ a]_. (1972) and Morrison (1975) have demonstrated 
that vampires and fruit bats avoid flying during intense moonlight, 
whole-ni ght samples were taken only between the last and first quarters 
of the moon. Only such whole-night samples were used to calculate 
species di versi ty, and activity cycles were taken during phases of the 
lunar cycle that do not produce enought light to influence bat flight 
acti v i ty. 

Nets and traps were, checked at least twice every hour for the 
purpose of removing bats. Whenever possible, checks were made more 
frequently to prevent bats from chewing out of nets. Upon removal from 
a net or trap each bat was placed in an individual cloth bag. Usually 
within an hour after capture the bats were banded and released at the 
sampling, station. The following data were recorded for each individual: 
species, hour of capture, capture location, sex, age class, reproductive 
condition of females, food in feces or mouth, weight, and forearm length, 



10 
Age classes were distinguished as follows. Infants were unable to 
fly and were encountered only when carried by the mother. Juveniles were 
able to fly but still had the infant pelage. Subadults had the adult 
pelage but were smaller in weight than adults and were reproduct i vely 
immature. Adults possessed both adult pelage and weight. 

Pregnancy, lactation, and reproductive inactivity of adult females 
were determined by palpation. Additionally, females could be distin- 
guished as nulliparous or post- lactat i ng by examining the condition of 
the teats. 

Fecal pellets obtained from individual animals were placed in 
separate glassine envelopes for laboratory identification of food 
species. Fruits and pollens in fecal pellets were identified to species 
by comparing unknowns with seeds, pulp fibers and pollen grains in a 
reference collection assembled by the author. Pellets were collected 
from insectivores but remain unidentified because the hard parts of 
arthropods eaten by bats are masticated into tiny fragments that are 
difficult to identify. Pollen on the fur was collected by swabbing 
with a gelatin described by Beattie (1971). The pollen-containing 
gelatin 'was then melted on slides for microscopic identification. 
Frequently, animals were captured with whole fruits held in the mouth. 
Additional information on food habits was gathered by placing plastic 
sheets under two roost trees of Carol 1 ia perspeci 1 lata to gather 
discarded fruits and fecal matter. 

Mathemat ical Formulae 
(1) Species Diversity, H 1 = -£P] log e pj, where pj is the number of the 
ith species divided by sample size (Shannon and Weaver, 1 949) . 



11 

(2) Equitabi 1 ity, E - H'/H max) where H max is the natural logarithm of 
the number of observed species (Sheldon, 1969). 

(3) Niche breadth, log e B = -£pj log e pj, in which the functions are 
the same as described in Equation 1. Values approaching zero indicate 
narrow niche breadths and specialists. Values approaching one indicate 

wide niche breadths and general ists (Levins, 1968). 

a 2 2 

(A) Niche overlap, CA= 2 Z Xj Yj/E Xj " + Yj , where X, is the propor- 
tion of the ith food species in the diet of bat species X, and Yj is the 
proportion of the ith food species in the diet of bat species Y (Morista, 
1959). I follow Zaret and Rand (1971) in considering species with over- 
lap values greater than 0.6 to be critically similar in terms of food 
overlap. 



PHENOLOGY OF FOOD RESOURCES 

Most of the bat species on Barro Colorado depend largely on fruit, 
flowers, or insects as food resources. Only a few species feed on the 
flesh or blood of vertebrates or non-insect invertebrates. The abundance 
and diversity of fruits, flowers, and insects in Central America, even 
in moist and wet forests, strongly fluctuate on a seasonal time scale 
(Foster, 1973; Smythe, 1974; Frankie et ajL , 1974), 

Pollen and nectar on Barro Colorado are available to bats as reliable 
food sources only in the dry season, and only four species of flowering 
plants are known to be used by bats (Table l) . Two common species, 
Ochroma 1 agopus and Pseudobombax septenatum , flower from mid-December to 
mid-March. While these two species are in bloom nectar and pollen are 
very abundant. The other two pollen types used by bats remain unidenti- 
fied. One of these is known only from February-March sampling and the 
other from August-September. 

Fruits from ^5 plant species were found to be eaten by bats on the 
island (Table 2). Nineteen of these species were trees, 11 were shrubs, 
four were vines, four were epiphytes, and seven are unknowns. Mature 
fruits of the species eaten by bats are available all year. There are 
times, however, when few fruits of only a few species are available. 
During 1973 a maximum of 19 fruiting species was available from mid- 
March to mid-April, and a minimum of 6 species was available in November- 
December (Table 2). Two of the fruits available in November- December , 

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16 

Ficus ins i pi da and £. yoponensis, were very scarce, but Spondias 
rad l kofer i and S. morobin were quite abundant. 

Most of the plant species producing fruits eaten by bats produce 
ripe fruits for periods of only one to four months. Only three species, 
L' ins ipi d a , _F. ob tus i fo l ia , and F. yoponen s is , have ripe fruits avail- 
able nine or more months per year. Individuals in the populations of 
these fig species fruit asynchronously once or twice per year. 
L- insipida and £. yo po nens i s populations show three major fruiting peaks 
and troughs each year (Morrison, 1975). 

The plant genera Cecropia, Spond ias , Vi smi a , and Pi per each have 
two or more bat"dispersed species that set fruit in sequential time 
periods (Table 2). There are 10 species of pipers on BCI eaten by bats. 
Though no one of these species is available for more than a few months, 
two or more species have ripe fruit throughout the year. Heithaus et al . 
(1975) report that pipers are important bat fruits in Costa Rica and 
that several species are available in similar sequential series. Snow 
(1965) reports that 18 species of the bird-dispersed genus Mic onia are 
sequentially available throughout the year in Trinidad. 

The biomass and numbers of nocturnal insects caught in light traps 
in Barro Colorado forest over a three-year period were reported by Smythe 
(197A). Though these samples represent all nocturnal flying insects, 
not just those eaten by bats, they provide a useful index of the abun- 
dance and fluctuation of the potential food resources for insectivorous 
bats through the year (Fig. 3). The light trap collections show that 
nocturnal insect biomass in the early wet season is as much as eight 
times that of the biomass at the end of the wet season and during the 
dry season (Fig. 2). Large insects (>5 mm in length) were responsible 



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19 
for this seasonal change in biomass, with Isoptera, Diptera, and 
Lepidoptera among the orders eaten by bats that have particularly drama- 
tic population increases in the wet season. By contrast, small insects 
(< 5 mm in length) were abundant throughout the year. 



SPECIES DIVERSITY 

Considerable variation occurred in the bimonthly measures of species 
diversity (Table 3)- All three diversity indices, H ' , E, and SN, were at 
maxima during the dry-to-wet transition sampling period. The three diver- 
sity measures then declined in each of the next three bimonthly periods 
to a minimum in the late»wet season. Whereas 27 bat species were present 
in the study area in the dry-to-wet transition, only 13 species were 
sampled in the ]ate*wet season. During this same interval H 1 dropped 
from 2.33 to 1.52 and equitability from 0.707 to 0.515- In the wet to 
dry transition period the diversity values began to increase. Dry season 
values were very similar to wet-dry transition values, but SN increased 
from 22 to 25 in this period. 

The diversity values were lowest in the mid- and late-wet season 
samples because 13 of the species common in the dry season became notice- 
ably rare or absent (indicated by asterisks in Appendix 1) from the study 
area in'one or both bimonthly periods. These include seven insectivorous 
species (hj% of the total insectivorous species), five frugivorous 
species (k2%) , and one nectar i vorous species (50%). These species appear 
to move to other habitats precisely at the time when bat-dispersed fruits 
and nocturnal ly flying insects, the two most important food resources for 
bats in this community, become relatively scarce on the study site (Fig. 
2 and Table 2) . 

Of the seven insectivorous bat species that move out of the 
mature forest late in the wet season, six are foliage gleaners and one 

20 



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22 

is an aerial hawker. The foliage gleaners prey chiefly on large insects 
such as cicadas, grasshoppers, and roaches (Wilson, 1571b; this study). 
Smythe (197*0 has shown that large nocturnal insects (greater than 5 mm 
in length) become quite scarce on this same study area beginning in the 
middle of the wet season, whereas small insects (smaller than 5 rnm in 
length) are relatively constant in abundance through the year. It 
appears that the foliage-gleaning bats find food resources in the study 
area sufficiently depressed in the latter part of the wet season that 
they move out of the area. On the other hand, small insects remain an 
abundant food resource ; and aerial feeding bats remain in the 
mature forest of Barro Colorado all year. P eropteryx kappleri , an 
aerial feeding bat, is an exception as it does move out of forest habitat 
in the late wet season. 

Of the two bat species that are primarily nectar i vorous in this 
community, Glossophaga so ricina switches from pollen and nectar to fruits 
and insects in the early wet season and then moves out of the area in the 
middle wet season, not to return until bat flowers appear in the dry 
season. Phyllostomus discolor stays in the area the entire year, sub- 
sisting on fruits and insects during the wet season. 

Among the fruit-eating species that seasonally move in and out of 
the Barro Colorado mature forest is Vampyressa pusilla , the smallest 
species of the 13 frugivorous bats on BCI. V_. pus ilia is a feeding 
specialist on small fig fruits. This bat left the study area when few 
individuals of its most important food species, F i cus yoponens i s , were 
producing fruits in July-October and returned in November when mature 
£.• yoponens i s fruits were again abundant. While specific reasons why 
other frugivorous species moved in and out of the study site are unclear, 



23 

their absence in September-November corresponds with the annua] period 
when few food plants are producing fruit (Table 2). 

The abundance of individual bats on the study area, as measured by 
the number of bats captured per sampling-hour, showed a pattern of 
seasonal change markedly different from the diversity measures pattern. 
Bats were captured in greatest numbers relative to sampling effort in 
the dry-to-wet transition, 0.425 bats/hr, and in the late wet season, 
0.423 bats/hr (Table 3). The large numbers of bats captured in the dry- 
to-wet transition sampling reflect large populations. Food resources 
were abundant then; females of most species were in the latter stages of 
lactation; and juveniles were entering the flying population and learn- 
ing to forage. These latter two activities are among the most energet- 
ically demanding in mammalian life cycles (Miguel a, 1969; Studier et al . , 
1973), and the timing of these costly activi ties seems geared to a period 
of food abundance. 

The late wet season peak in capture rate does not solely reflect 
large numbers of individuals on the study area. Though a number of 
species had at this time moved out of the young forest, some of the 
remaining frugivorous species were recruiting juveniles into the flying 
population from the second birth pulse of the year. Probably much of 
the high capture rate is attributable to intense foraging activity 
necessitated by low food supplies. 

The diversity values for insectivorous and frugivorous species, 
when computed separately, change similarly through the seasons (Table h) . 
For both groups, species diversity is high from mid-November through 
mid-July and low the remainder of the year. Fruit bat diversity rises 
and falls in time as does the diversity of fruit (see Table 2). However, 



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25 

insectivore bat diversity sharply rises four months before, insect biomass 
explosively increases (see Fig. 2). The latter anamoly may be due to 
ineffective harp trap placement and particular under-representat ion of 
the abundant species, Pteronotus parnel 1 i i , during the first months of 
field work. This would cause the dry season diversity value to be higher 
than it should be. Most species of fruit bats remain in the BCI mature 
forest habitat throughout the year. On the other hand, the species 
number of insect-eating bats in the dry-to-wet transition is nearly 
double that, of the late wet season because of the movement of foliage- 
gleaning species in and out of the forest. 

A measure of annual variation is achieved by comparing the diver- 
sity of frugivorous species in June, July and August of 1971, 1973, and 
197^ (Table 5). In all three years there is a consistent trend toward 
lower diversity as the wet season progresses. However, the magnitude 
of the diversity values varies from year to year. This indicates that 
some annually variable factor or complex of factors, possibly food 
availability, predation, or reproductive success, influences fruit bat 
species diversity. Insectivore diversity is not compared because harp 
traps for effective sampling were available only in 1973- 



26 



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RESOURCE PARTITIONING 

Thirty-five species of bats were found to coexist on Barro Colorado 
Island in 1973= Thirty-one species were captured in diversity samples 
and four additional species were seen in flight or at roosts. Nocti 1 io 
lepor inus , N_. labial is , and Mo l ossus molossus restricted their flight 
activities to habitats that were not sanipled--the shallow inlets of the 
lake ( Nocti 1 io ) and above the. forest canopy ( Molo ssus) . The fourth 
species not captured in the diversity samples, V ampyrum sp ectrum , is a 
top carnivore and may be represented by very 'few. individuals on the 
island. A pair of V. spectrum was netted by A. L. Gardner and D. E. 
Wilson on 5 January 1973- I saw a single animal in June 1973 flying at 
dawn. No other sightings of V_. spectrum were reported in 1973- 

A first step at understanding how 35 species of bats coexist on 
this small island can be made by dividing the fauna into feeding guilds. 
Feeding guilds will be distinguished on the basis of two parameters- 
general 'food type and method or place of food procurement. It will be 
assumed that little or no competition for food resources occurs between 
members of different feeding guilds, though they may compete for roost- 
ing space. The bats on Barro Colorado may be divided into nine feeding 
guilds, each of which contains one to nine species. 

Justification for the placement of species into specific feeding 
guilds will be provided in succeeding sections. For the moment, the 
feeding guilds are defined as follows: 

(1) "Canopy frugivores" -- forage mostly on fruits that grow in 

27 



28 
the trees of the canopy and subcanopy level of the forest, above 3 m from 
the ground. 

(2) "Groundstory frugivores" -- forage mostly on fruits of shrubby 
ground story plants, to 3 m above ground level. 

(3) "Scavenging frugivores" -- feed mostly on over-ripe fruit. 

(A) "Nectar-pol len-frui t- insect omnivores" -- forage for pollen and 
nectar from flowering trees when available in the dry season and then 
switch to a fruit and insect diet in the wet season. 

(5) "Sangui vores" -- feed only on the blood of mammals and birds. 

(6) "Gleaning carnivores" -- forage for small animals (arthropods 
or vertebrates) that are perching or moving on vegetation or on the 
ground. 

(7) "Slow-flying hawking insecti vores" — forage for flying insects 

i 

in small openings beneath or in the forest canopy or over streams. 

(8) "Fast-flying hawking insect i vores" — forage for flying insects 
above the forest canopy or in very large open spaces. 

(9) "Piscivores" — forage for fish or aquatic invertebrates at or 
just above the surface of lakes and large streams. 

The distribution of mean body weights for each bat species on 
Barro Colorado by guild is plotted in Figure 3. Three guilds contain 
a single, species, and I expect that each of these species is sufficiently 
unique to preclude serious interspecific competition for food. The 
species within the groundstory frugivore, canopy frugivore, and piscivore 
guilds increase in body weight with a geometric progression factor of 
about 1.J to 1.8 (with one exception in the canopy frugivore guild). 
We might expect that the species within each of these guilds exploit 
very similar types of food, captured in very similar manners, and that 



Figure 3. Mean body weights of bat species by feeding guilds, 
(Dashed lines separate members of different families that belong to the 
same feeding guilds.) 1. Carol 1 ia castane a, 2. C. perspeci 1 lata , 
3- Vampyressa pusi 1 la, 4. Chiroderma trim tatum . 5. Artibeus phaeotis, 
6- Vampyrops hel leri , 7, Ch i roderma vi 1 losum , 8. Vam pyrode s caracciolo i , 
9- Artibeus jamaicensis, 10. A. 1 i turatus, 11. Centurio senex, 12. Glossc 



phaga soricina , 13. Phyl lostomus disc olor, \k. Phyl lode rma sTenops , 
15. Desmodus rotundus , 16. Micronycte r is mega 1 ot i s ,17. M. brachyotis, 
18. Mimon crenu latum , 19. Mi cro nycter i s hirsuta , 20. Trach ops cirr hosus , 
21. Tonat ia sylvicola, 22. T. bidens , 23. Phyl lostomus hastatus , 2k. Vampy- 
rum spectrum , 25. Rhogeessa tumida, 26. Myotis nigr icans , 27. Saccopteryx 
leptura, 28. Centronycter i s maxim? 



i an i 



29. 



Saccopteryx b i 1 ineata , 
30. Peropteryx kappler i , 31. Pteronotus suapurensis , 32. _P_" 
33. Molossus mo loss u s, 34. Nocti 1 io labial is , 35. N. lepo7inus" 



oarnel 1 i i 



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31 
food resources are partitioned largely by particle size as predicted by 
the theoretical reasonings of Hutchinson (1959), McNab (1971a ar >d b) and May 
0973). These authors postulate that similar species may avoid competi- 
tion for food by differing in body weights by a factor of at least 1.3 
(May, but McNab and Hutchinson used the figure 2.0), each species 
specializing in food particles proportional to its body weight (and to 
the linear dimensions of its food handling apparatus, e.g., tooth row 
length, gape size, tongue length, etc.). 

The gleaning carnivore and slow-flying hawking insectivore guilds 
each contain some species that are very similar in size to other species 
of their guilds. We might expect that such species feed on similar- 
sized food particles of very different taxa or of similar taxa from 
different microhabi tats. 

The nectar-pol len-frui t- insect omnivore guild contains species very 
different in size; this may partly result from a recent extirpation of 
Lonchophylla robusta , a species intermediate in size between Glossophaga 
soricina and Phyllostomus discolor . The sexual dimorphism in body 
weights of JP. di scolor is another complicating factor. 
Canop y Frugi vore Gu i Id 
Body s ize 

Eight species, all in the subfamily Stenoderminae of the Phyllosto- 
matidae, constitute the canopy frugivore guild on Barro Colorado. These 
eight species range from 8.1 to 69-3 g in mean body weight (Table 6). 
There is a mean increment of ].hk between the body weights of adjacently 
sized animals among the seven species designated as fig feeding 
specialists in Table 6. A rtibeus phaeotis , a feeding general ist, and 
Chiroderma trinitatum are nearly the same in size. 



32 



Table 6. Wefghts fn grams of canopy frugivore bats on Barro Colorado. 



Species 



Sample Sample Wgt / Wgt* 
Mean size size lg sm 
(x) (S.D.) n 



Remarks 



1- P usMla 8.1 0.6 

C. trinitatum 12.3 1.2 

A. phaeotis 1 3.0 1.2 

1- helleri 16.2 2.2 

£. vil losum 22. k 2.1 

V_. caraccioloi 36.0 2.3 

A. jamaicens is 47-2 3.4 

A. 1 ituratus 69.3 5.6 



22 

7 
30 

8 

13 
27 
30 
30 



1.53 

1.31 
1.38 
1.61 
1.31 
1.47 



Fig special ist 

very rare fig specialist 

food general ist 

very rare fig specialist 

fig special ist 

fig special ist 

fig special ist 

fig special ist 



mean ratio of weight increment=l .44 



-Weight of larger species divided by weight of smaller species 
in the pair compared. 



33 
Food select ion 

All eight canopy frugivore species feed primarily on fruits of 
large canopy and subcanopy trees, in particular figs of the genus Ficus. 
Over 60? of the annual diet (by frequency of occurrence in fecal matter) 
of seven of these bat species consists of fig fruits (Table 7); these in- 
clude £. trinitatum , but not A_. phaeotis of the same weight. A. phaeotis 
depends on figs for 30? of its diet. Five species of Ficus , all of which 
are green colored at maturity, are eaten and dispersed by these steno- 
dermines on Barro Colorado. Fig species that produce large fruits are 
preferred by large bats, and fig species that produce small fruits are 
preferred by small bats. 

Figs form the bulk of the diet of Artibeus jamaicensis throughout 
st of the year. However, during the latter part of the wet season 
nd the very beginning of the dry season mature fig fruits are very 
scarce (Morrison, 1975). At this time A. jamaicensi s turns more heavily 
to other fruits and pollen (Table 8). The relative importance of pollen 
in the diet of A. jamaicensis is grossly underestimated here because my 
sampling schedule did not coincide with the two weeks in late December 
and early January when figs were very scarce and flowers were very 
abundant. Similar seasonal switches in diet also probably occur for 
A- 1 ! turatus and V_. caraccioloi « but the data are weak. No conclusions 
can be made from the scant data on the smaller species of canopy frugi- 
vores with respect to seasonal switches in diet. 

Unlike the fig specialists, A. phaeotis eats a more even distribu- 
tion of many types of fruits (Tables 7 and 8) with no one species 
strongly dominating the diet. Throughout the year figs are a minor 
component of the diet, while other fruits are very important in certain 



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35 



Table 8. Bi-monthly samples of important food species in the diets 
of Artfbeus and Vampyrodes . Sampl ing periods begin at 
mid-month. 

Food Species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan 



Art ibeus jama icens is 

Ff cus spp. 18 25 25 35 21 17 

Cecrop la spp. 3 3 

Spond ias spp. j g g 



Quarar ibea 



9 



Pollen 1 

Total feeding samples- 20 30 32 39 35 37 

Art ibeus 1 ituratus 
Ficus spp. 2 4 1 1 it 

Spondias spp. ) ] ^ 

Pollen 1 

Total feeding samples- 3 If 5 2 7 

Art ibeus phaeot is 
F ' cus spp. 2 12 13 

Cecropia spp. 1 5 

Spondias spp. o 

Total feeding samples- 5 6 9 111 

Vampyrodes caraccioloi 
F 'cus spp. 12 k 31 

Pollen 2 

Total feeding samples- 3 3 k 3 



-Includes genera of lesser importance not shown here, 






36 

months. Cecropia exima is an important food item from July to September, 
as is Spondias radlkoferi in November to January. 

Feeding niche breadths based on food species by frequency of occur- 
rence in the diet are presented in Table 9. Large niche breadth values 
represent food general ists and small values food specialists. 
A_. phaeo t i s stands alone at the general ist extreme of this index. 
A- j'ama icens is has an intermediate position between the general ist and 
the extreme specialists. The remaining six species are bunched as 
extreme specialists. Hereafter, all members of this guild will be 
referred to as "fig specialists" except for the feeding general ist, 
A. phaeot i s . 

Niche overlap in food species is compared in Table 10. The highest 
values of overlap in canopy frugivores occur between species most similar 
in size (diagonal left edge of Table 10). A. phaeot is overlaps little 
with all the fig specialists, except for V_. hel ler i , which is similar 
in size. The high values of overlap between many of the fig specialist 
species indicate that some mechanism other than selection of food 
species must be operable to reduce behavioral interference and/or inter- 
specific competition for food in this guild. 

Several types of evidence strongly suggest that food is a limiting 
factor for fruit bats on Barro Colorado, at least during some parts of 
the year. The biomass of fruit and the number of species of fruiting 
trees fluctuate quite drastically on a seasonal basis (see Phenology 
section). During the late wet season fruit availability is low,and an 
increased proportion of captured fruit bats have empty stomachs (83% in 
Oct-Nov) as compared to times of fruit abundance (71% in Mar-Apr). 



37 



Table 9- Feedfng niche breadths of canopy frugivores. 



Bat Species Number of genera of Number of species of Niche Breadth* 

known food plants known food plants (log B) 



2 4 0.94 

3 4 1.33 
10 12 2.10 

2 3 1.01 

1 3 1.01 

4 5 1.04 
9 16 1.61 

5 7 1.33 



V. 


pusi 1 la 


c. 


tr in i tatum 


A. 


phaeoti s 


V. 


hel ler i 


c. 


vi 1 losum 


V. 


caraccfoloi 


A. 


jama icens is 


A, 


1 i turatus 



'Sample sizes for calculating niche breadths are as in Table 7. 



38 



Table 10. Feeding niche overlaps (CA ) among species of the 
canopy frugivore guild 



ha 

c 

Ln 
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A_. phaeot is 

\l_. pus ?lla 

C_. trin i tatus 

V. helleri 



.215** 



C_. v? 1 losum 
V_. caraccioloi 
h.- jamaicens i s 
A. 1 i turatus 



354* and 


.615**" 


.241** 


.465** 


.485** 


.518 


.968* 


.452 


.796 


.679 


.272 


.152 




.893* 


■ 743 


.644 


.209 


.412 






.798* 


.886 


.852 ' 


.452 








.727* 


.200 
.994* 


.310 
.962 
.983 



Denotes species most similar in body weight 
Denotes overlap with the feeding general ist 



39 

Also by the late wet season several species of fruit bats have tempo- 
rarily moved out of the study area, and the remaining individuals and 
species spend a greater part of their nightly time budgets in foraging 
(see Species Diversity section). Even when fruit is very abundant in 
terms of total biomass, it is concentrated in a limited amount of 
space, the few trees fruiting at any moment, and may still be a limit- 
ing factor for population size. 
Vertical stratification 

Handley (1967) and Harrison (1962) demonstrated a vertical strati- 
fication of flight activity in Neotropical bat species, with most canopy 
frugivores preferring upper levels of the forest. On Barro Colorado, 
h pusilla , A. phaeotis , C_. vi llosum , V. caracciol i , and A. 1 ituratus_ 
were captured with highly significant frequency in the nets and traps 
set above 3 m (Table 11). V. helleri and £. trinitatum also were 
captured most frequently in subcanopy-canopy levels, but sample sizes 
for these species are small, and frequency differences are not statis- 
tically significant. A. jamaicensis is the only species of the guild to 
"show a significant preference for activity at the groundstory level, 

yet k2% of the captures of even this species were in the upper levels 
■ of the forest. Though most of its food items grow in the upper levels 
of the forest, A. jamaicensis may fly close to the ground to avoid 
predators. On the other hand this behavior may be an artifact of the 
human management of the forest, with this species opportunistically 
finding it more efficient to fly along cleared trails than to repeat- 
edly detect and avoid vegetation at higher levels. 



ko 



Table 11. Vertical stratification of canopy frugivore species on 

Barro Colorado. Statistical significance indicates pref- 
erence for one of the two vertical strata. 



Bat Species 



No. of bats captured at No. of bats captured at 
ground level, to 3 mm subcanopy levels, 3 to 12 mm 



V. pus ilia 



c. 


trinitatum 


A. 


phaeot is 


V. 


hel ler i 


c. 


vi 1 losum 


V. 


caraccioloi 


A. 


jamaicens is 


A. 


1 ituratus 







5 

2 

36 

3 

h 

2,67** 
23 



25- 

h 

56* 

6 

30*- 

326 

66* 



* Significant by Chi Square Test (P_ <.05). 

** Highly significant by Chi Square Test (_P <. .01). 

Yates Correction for Continuity is used on all tests of samples 
with N< 200 (Sokall and Ron If, 1969). • 



1*1 

Habi tat selection 

Comparison of netting samples from the young open forest of Buena 
Vista and the closed canopy forest and creek habitats of Barro Colorado 
provide a measure of species preferences for three habitats (Fig. k) . 
As a group the fig specialists are much more common in the closed forest 
and creeks lined by closed forest than in the shrubby open forest where 
few mature trees of their preferred food species are found. A. phaeotis 
and A. jamaicensis are common to very abundant in all three habitats, as 
would be expected from their more generalized food requirements. None 
of the extreme fig specialists are common on Buena Vista Peninsula. 
Feed ing behavior 

Canopy frugivores usually carry fruits by mouth from fruiting trees 
to night feeding roosts (Goodwin and Greenhall, 1961; Morrison, 1975). 
On BCI Morrison found that the night feeding roosts of A. jamaicensis 
are frequently several hundred meters away from the fruiting trees where 
they. are picked. Only when feeding on the large fruits of Dipteryx 
panamensis did Artibeus feed on fruiting trees. All four most common 
canopy frugivore species were observed to carry whole or partially eaten 
fruits in flight. These animals presumably were transporting food items 
to a night feeding roost for consumption. Whether the less common 
species in the guild use night feeding roosts is unknown. 

The fruits carried in flight by fruit bats vary in weight from less 
than 1 g to about 20 g. Most bats carry fruits that weigh 20 to k0% of 
their own body weight. Table 12 lists the range in weights of some 
fruits eaten by stenodermine bats. There is considerable variation in 
the weights among and within species for these fruits (even in fruits 
from the same individual tree). 



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O 

~CN 
CO 



CO 

CN 



~o 

CO 

"o 

CN 
CO 

~o 



CO 

CM 

o 



CO 
LU 

o 

LU 

Z) 



T "F T * " * * 



I 



CN 
lO 

_CN 

CO 
_CN 

O 
CO 

CN 
CN 

'f 

CO 

J-"-* 

•o 

O 

_CN 

~o 



o 

_CN 

<3 

_CN 

CN 
CN 

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to 

o 



CN 



:-i CN 
:1 co 



— r~ 

o 

CN 



- r~ 

o 



O 



VNOYJ JO !N3Dci3cl 



Table 12. Wet weights in grams of some fruits eaten by bats on 
Barro Colorado Island that were collected beneath 
fruiting trees. 



44 



Plant Species 



Fruit Weights 
Range Mean S. D. 



Ficus ins ipida 
Ficus obtus J fol ia 
F icus yoponens is 
Anacard i urn excel sum 
Calophyl 1 urn long? fol i urn 
Dipteryx panamens i s 
Spondfas radl kofer i 
Quararibea asterolepis 
Astrocaryum standi eyanum 
Piper cordul atum 



7. 1-11. 4 


9.1 


1.5 


10 


14.2-19.0 


17.0 


2.5 


3 


1.5- 5.6 


3-1 


1.1 


12 


4.2- 6.2 


5.1 


0.7 


7 


9-3-17.7 


14.7 


3-3 


7 


18.0-26.3 


22.3 


3-6 


5 


8.6-13-0 


10.6 


1.4 


9 


4.9- 6.3 


5.45 


0.6 


4 


17.0-20.5 


18.8 


1.8 


4 


0.5- 2.0 


1.2 


0.5 


15 



h5 
Food particle size plays an important role in the partitioning of 
food resources among similar species in many types of animals (e.g. 
Diamond, 1973; Brown and Lieberman, 1973) and may be particularly impor- 
tant for fruit bats because of the behavior of carrying fruits in flight 
to feeding roosts. According to the theory of optimal foraging strategy 
(Schoener, 1 969) , each bat should attempt to maximize the amount of food 
it harvests per unit of time and thus select the largest food particles 
it can efficiently find and handle. The weight that a bat can carry in 
flight without seriously impeding manuverabi 1 i ty probably sets the upper 
limit on food particle size for these animals. 

Figure 5 shows that there is a highly significant correlation (by 
F distribution, P <.01) of fruit weight with bat weight for fruits 

„ MM 

carried into nets by the three largest species of bats in the canopy 
frugivore guild. Most of the points in this figure represent Ficus 
insipida fruits, the most important food species in the diet of all 
three bat species. Thus even though these three bats have high overlap 
in food species (Table 10), they are able to specialize on food particle 
sizes proportional to their body weights. The smaller canopy frugivore 
species probably do the same thing, but no data are available. 

Each species in the canopy frugivore guild has a distinct cycle of 
flight activity. The three largest species, _V. caraccioloi , A. jamai- 
censis , and A. 1 ituratus , each have their greatest peaks in activity at 
different times of the night (Fig. 6). Since all three of these species 
feed largely in the same individual trees in the course of the night, 
the offsetting cycles of activity probably function to minimize inter- 
specific aggression from crowding at the resource trees, especially 
when resources are concentrated in a few trees per night. Reduced 



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Sd!D3dS HDV3 dO IVIOI dO !N3D>i3d 



50 
crowding at resource trees presumably is of importance in permitting more 
efficient feeding and in making these bats less obvious to the many kinds 
of arboreal and aerial predators that eat bats (Humphrey and Bonaccorso, 
1975). 

A similar pattern of offsetting major activity peaks should be 
expected in the small canopy frugivores, all of which feed heavily on 
Ficus yoponensis and F_. popenoaei . Figure 7 shows that V. pus ilia is 
most active in the first two hours after sunset, and C_. vi 1 losum is most 
active later in the night. Paucity of data prevents comparison of the 
other small fig specialists. 

A- phaeot i s , the feeding general ist, has a much more even distri- 
bution of activity through the night than any other species (Fig. 7). 
Many of the fruits eaten by A_. phaeot i s are not eaten by other stenoder- 
mine bats and it need not compromise its activity cycle to avoid crowded 
resource trees. 
Groundstory Frug i vore Gu i 1 d 
Body size 

Two species in the subfamily Carol linae of the Phyl lostomat idae 
constitute the groundstory frugivore guild on Barro Colorado. They are 
Carol 1 ia castanea and C_. perspi ci 1 lata . These have mean body weights 
of }2.k and 17.9 g> thus differing in body weight by a factor of 1 .hk 
(Table 13). 

A few individuals of a third species of the genus Carol 1 ia , 
C_. subrufa , were captured and banded by R. K. LaVal in 1972 on Barro 
Colorado (pers. comm.). In 1973 and 197^ I recaptured some of LaVa 1 ' s 
banded C_. perspici 1 lata and £. cas tanea , but I have not encountered any 
of the C_. subrufa he marked. It is difficult to distinguish 



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a) 


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S3iD3d$ H3Y3 .IO IViOl dO iN33^3d 



53 



Table 13- Weights of groundstory frugivore bats on Barro Colorado 



Bat species 



Mean Standard Sample Weight of larger species 
(x) deviation size divided by weight of 

smaller species in the 
pa i r compared 



C. castanea 12.4 



C. perspici 1 1 ata 17-9 



1.8 
1.8 



30 
30 



M 



5k 

C. perspicillata and C. subrufa by field characters, and it is possible 
that I lumped a few individuals of C_. subrufa with C_. perspicil lata 
because I was not aware that C_. subrufa was present on BCI. I believe 
C. subrufa is very rare on Barro Colorado, and lumping a few of them 
with C_. perspicillata would influence the data on this latter species 
to a very minor extent. 
Food selection 

C. castanea and C_. perspici 1 lata are food general ists in that they 
eat a fairly even distribution of a large number of kinds of fruits and 
have large niche breadth values (Tables 14, 15, and 16). Though no one 
food species dominates their diet in any one season or over a long 
portion of the year, eleven species of the shrubby plant genus PJ_per 
(Piperaceae) constitute the bulk of the diet of £. castanea and nearly 
one-third of the diet of C_. perspicillata . Ten species of pipers were 
identified in the fecal samples from C. castanea and nine species from 
C. perspicil lata . At least one species of piper is available with 
mature fruit in every month of the year on Barro Colorado (see Table 2). 
C. castanea eats pipers all year long, but no pipers were evident in the 
diet of £. p erspicillata from mid-September through mid-November. 
c - perspici llata appears to feed exclusively on subcanopy and canopy 
fruits in the late wet season. Particularly important are Solanum 
haysei i , Quararibea asterolepis and Cecropia exima . Other fruiting 
trees are important food species along with pipers at other seasons. 
Though fruiting shrubs dominate the diet of C. castanea , fruiting trees 
are somewhat more important than shrubs for C_. perspici 1 lata . 

In addition to the fecal samples from captured animals, food habits 
data for jC, perspicil lata were obtained by monitoring droppings bel° 



low 



55 



Table lit. Food species in the diet of C. castanea as determi ned f rom 
frequency of occurrence of seeds in fecal samples. Sampling periods 
begin at mid-month. 

Plant species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan Total 



Piper aequale 
P. cordulatum 



P. reticulatum 


1 




P. marginatum 


3 




P. carrilloanum 


} 


1 


Piper 109 


1 


Piper ]]k 






Piper 120 






Piper 122 






Piper 150 







Unknown 104 
Unknown 123 



Shrubs 



1 

3 
2 
Trees 



Carl udovica pal mata ' 

Sol anum haysei i * 

Markea panamens is 
Vismia 1 



Brosimum bernadettae ' 

Dipteryx panemens is 1 

Aechmeia ti 1 landsoides 1 



Unknown 



3 3 6 15 

1 9 

3 1 5 

1 1 6 

1 2 

2 h 

1 1 

1 2 

3 
2 



1 
2 

9 11 11 

2 1 3 



1 
1 
1 

1 
1 



56 



Table 15. Food species in the diet of C_. perspici 1 lata as determined from 
frequency of occurrence of seeds in fecal samples. Sampling periods begin 
at mid-month. 



Plant species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan Total 



Shrubs 



Piper aequale 1 ] 

P_. cordulatum 10 1 11 

P_. ret iculatum 7 7 

P_. marginatum 111 3 

Piper 109 k 1 16 

Piper \\k 1 1 2 

Piper 116 1 ] 

1 3 
2 



Piper 120 






2 


Piper 150 






2 
Trees 


Carludovica palmata 






1 


Solanum haysei i 


1 


G 


1 


Markea panamensis 


1 




h 


Vismia 1 






h 


Vi smia 2 




1 


1 


Cecropia exima 




1 




Brosimum bernadettae 




3 




Quararibea asterolepis 








Dipteryx "panamensis 


7 


1 




Cassia undulata 




3 





} 

3 
5 
9 
2 
3 
3 
6 
8 
3 



57 
Table 15, continued. 

Plant species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan Total 



Unknown 101 1 j 

Unknown 103 1 1 

Unknown 10^1 1 

Unknown 125 k k 

Unknown 127 2 2 

Insects 5 1 fi 



58 



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59 

two day roosts of this species. Both roosts were in hoi low Anacard i um 

excel sum trees. With the exception of _A. excel sum a 1 1 common food items 
identified from the day roost droppings appeared as important food items 
in the fecal samples from captured bats during the same bimonthly 
periods (Table 17). 

Why did not A. excel sum ever show up in the fecal material from 
captured bats? Probably A_. excelsum is the only tree species that 
commonly serves as both a day roost and an important food resource for 
C_. persp ic i 1 1 ata ■ These bats need only fly to the canopy of the roost 
tree, pick a fruit, and carry it back inside the roost to eat it. The 
bats would usually digest and excrete the fruit before flying away from 
the roost to forage for other fruits; thus little chance would exist for 
this pulp to show up in netted animals. The Carol 1 ia colonies in 
A. excelsum trees consisted only of 6 to 8 bats and each colony probably 
had access to more A_. excel sum fruits when in season than they could eat. 

Anacardium excelsum is the only fruit I know to be eaten by bats 
on Barro Colorado that is not dispersed. Not only are the fruits carried 
within the hollow parent tree, but it is the single, large seed and not 
the fruit' pulp that is eaten. However, a few seeds probably are dis- 
persed when dropped by mistake. 

Overlap between the diets of the two Carol 1 ia is moderate in terms 
of food species. A CX value of 0.584 is obtained from lumping the food 
habits data from fecal samples from the entire year. Food overlap was 
very high in May-July sampling, CA = 0.798. This latter value, as well 
as the annual value of overlap, would be considerably smaller if it were 
possible to correct for Anacardium eaten in roost trees by C_. perspici 1- 
lata . Even though roosts were not monitored, it is unlikely that 



60 



Table 17- Frequency of occurrence of food species in the diet of C_. 
perspi ci 11 ata as determined from fruit droppings and seeds below day 
roosts. Sampling periods begin at mid-month. 



Plant species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan" Total 



Anacardium excelsum 5 83 39 127 

Piper cordul atum 39 35 9 83 

P. reticulatum ,6 6 



No data. 



83 


39 






39 


35 


3 






- 


6 


6 


1 






1 






2 


2 






5 


15 



Piper 109 6 6 

Solanum haysei i 1 1 2 

Vismia 1 2 2k 

Quararibea asterolepsis 5 15 20 

Cass ia undul ata 5 1 6 

Unknown 155 12 12 

Unknown R-l 3 3 






61 

C. castanea eats much of this fruit, as it is larger than all other 
important fruits in the diet of £. castanea . 
Habi tat selection 

Of the three habitats sampled, the Carol linae were most common In 
the second growth forest and least common in the mature forest, as are 
their most important food plants. £. castanea accounted for 21.7% of 
all bats captured in the second growth forest, 2.7% of the bats in the 
creeks, and 1.4% of the bats in the mature forest (Fig. 6). 
£. perspicillata constituted 15-8%, 16.0%, and $.k% of the bat individ- 
uals captured in those habitats. Whereas many species of pipers grew 
abundantly in the sunlight of the open canopy second growth and along 
the creeks (though less so along creeks), only one species, P_. 
cordulatum , was abundant in the shade of the mature forest. 
Vertical strati f icat ion 

C. castanea and £. perspici 1 lata were both captured more frequently 
at ground level than at upper levels of the forest (£. castanea = 20 
ground level, 14 upper levels; £. perspicil lata = 50 ground level, 
3 it upper levels), but the difference was not statistically significant. 
Both species feed on plants of ground and canopy levels. Known ground- 
story fruits make up 78.4% of the diet of £. castanea and 38% of the 
diet of £. perspici 1 lata . During seasons when £. perspici 1 lata is 
feeding mostly on canopy fruits, it also is captured more frequently 
in high nets and traps. 
Feed i ng behavior 

Carol 1 ia castanea and £. perspici 1 lata both have been captured 
carrying fruits in the mouth and presumably use night feeding roosts as 
do canopy frugivores. Some fruits are carried back to the day roost 



62 
for consumption as already discussed. The use of day roosts as feeding 

places by C_. perspici 1 lata is mainly a phenomenon related to feeding on 

one fruit, Anacardium excelsum , as is evident from the dominance of this 

fruit below day roosts and the decrease of dropped fruits and seeds when 

A_. excelsum is not in fruit (Table 18). It is likely that temporary 

night feeding roosts are used by these bats to avoid making the day 

roosts conspicuous to predators and to reduce flight distances between 

foraging forays. 

The flight activity of Carol 1 ia through the night is presented in 
Figure 8. Both species show major peaks of flight activity in the first 
hour of darkness. This is much earlier than the start of most canopy 
frugivores 1 flight activity and is probably due to the groundstory 
becoming dark about an hour before the canopy level of the forest. 
Cycles of flight activity in groundstory frugivores are bimodal or tri- 
modal as are those of canopy frugivores. Two or three such bouts of 
diel feeding activity also have been observed in fruit bats by Brown 
(1968) and LaVal (1970) and seem characteristic of bats that feed on 
foodstuffs that are not efficiently assimilated. 
Scaveng ing Frugi vore Gu i Id 
Body s ize 

Centurio senex (Stenodermi nae , Phy 1 lostomat i dae) , the wrinkle-faced 
bat, is the sole member of the scavenging frugivore guild. A lactating 
female weighed 22 g and a pregnant female weighed 27 g. No other weights 
are available from Barro Colorado for this species, nor are there any 
useful data on vertical stratification or habitat selection. 



4J 



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S3Q3dS HDV3 30 "1V101 3Q !N3Dd3d 



65 
Food species select ion an_d feeding behavior 

From several morphological features, particularly the small teeth 
and narrow esophagus, Paradiso (1967) concluded that C_. senex probably 
feeds on a "soft fruit or fluid diet". The small teeth, narrow esoph- 
agus, and lack of facial hair (like vultures) on this bat are suggestive 
of its possibly feeding on over-ripe or decaying fruit. Hence I tenta- 
tively designate it a "scavenging frugivore". The amount of rotting 
fruit on the forest floor is incredibly large on Ba'rro Colorado and 
potentially could provide an abundant food resource for such a bat. 
Goodwin and Greenhall (1961) mentioned finding fruit pulp in stomachs 
°f £• senex from Trinidad. Of the individuals that I captured on Barro 
Colorado one defecated an unidentifiable fruit pulp and the other carried 
a fresh Spondias radlkoferi fruit in its mouth. At this time it can 
neither be confirmed nor disproved that Centur io is a scavenging frugi- 
vore. Though it is very similar to Chi roderma vi 1 losum in body size 
I have no doubt that this anatomically unusual bat is ecologically quite 
different from any other frugivorous species on Barro Colorado with 
respect to food habits. 

Nee tar - Pol len - Fruit ~ lnsect Omn i vore Guild 
Body si ze 

The nectar-pol len-frui t- insect omnivore guild (hereafter referred 
to as the omnivore guild) contains three species, all of the family 
Phy 1 lostomat i dae -- Glossophaga soricina (Glossophag inae) , Phyl lostomus 
di scolor (Phyl lostominae) , and Phylloderma stenops (Phy 1 lostomi nae) . 
The mean body weight for P_. discolor on Barro Colorado is 4.36 times 
larger than that of G_. sor i cina (Table 1 8) , a larger difference than 
is found between species adjacent in size in any other guild. The large 



66 



^able 18. Weights fn grams of omnivore bats on Barro Colorado 



Bat species 



Mean 
(x) 



Standard 

Deviation 

(S. D.) 



Sample 
s ize 
(N) 



Wgt / Wgt * 
1 g sm 



G. soricina 



P. discolor 



9.8 
42.8 



male P_. discolor 44.6 

female P. discolor 39.7 

_P. stenops 61.8 



1.0 
3.9 
3.6 
2.1 



9 
27 
17 

10 
1 



4.36 



1 .42 



-Weight of larger species divided by weight of smaller species in the pair 
compared. 



67 

gap in body weight between G_. soricina and f\ discolor exists because 

of the recent extirpation of a bat species belonging to this guild. As 
recently as the early 1 950 ' s , Lonchophy 1 la robusta (Glossophag i nae) , 
was alive on Barro Colorado (Hall and Jackson, 1953). This species eats 
nectar, pollen, fruit, and insects (Howell and Burch, 1974). I, robusta 
from Costa Rica weigh about 17 g,and if this species were still present 
on Barro Colorado the ratios between body weights of the four omnivore 
guild members would be 1.4, 2.6, 1.4. The large ratio between L.. robusta 
and H' discolor actually would have been somewhat less than 2.6 because 
of the sexual dimorphism in body weights of P_. discolor . The dimorphism 
in body weights between male and female P_. disco lor is very slight (Table 
"1.8) but significant (P_<.05, Student's ftest). 
Food select ion 

Nectar and pollen are consumed by guild members almost exclusively 
in the dry season, as large flowers suitable for bat use are in bloom 
only then (see Phenology). The few data available suggest that during 
the wet season fruit and insects become dietary staples (Table 19). 
That insects were not present in the food samples from _G. soricina on 
Barro Colorado is probably because of poor sample size and the fact that 
this species moved out of the study area during the wet season. Nothing 
beyond the observations of Jeanne C 1 970) of f_. stenops eating social 
wasp larvae and my two observations of fruit eating is known about the 
diet of this bat. 

Phyllostomus discolor is neither an extreme specialist nor generalist 
in terms of food species (niche breadth = 1.65), Several types of flowers 
are visited for pollen and nectar in the dry season. And in addition to 
insects, several types of fruits are eaten in the wet season. The 



68 



Table 19. Seasonal use of pollen and fruit by the omnivore guild on 
Barro Colorado. 



Food species No. of dry season No. of wet season 

samples samples 



Pol len 



Cecrop ia exima 
Unknown 124 
Insects : 



Pol len: 



Fruit : 



Fruit : 

Unknown 1 10 
Unknown 151 



P.. discolor , N = 23 



chroma lagopus £ 

Pseudobombax septenatum 6 

Unknown 202 
Frui t" 



G. sor icina , N = 6 



Och roma lagopus 3 

Unknown 201 I 



2 
3 
3 



Cecrop ia exima 1 

Piper 109 , 

P_. stenops , N = 2 



69 
available data are too limited to consider niche breadth values for 
_P_. stenops and G_. soricina , or to calculate niche overlaps between 
gui Id members. 
Vertical strat if ication 

All of the flowers and fruits eaten by P_. discolor and 83% of those 
eaten by G_. soricina in this study area grow in the subcanopy and canopy 
of the forest. Both species were captured most frequently in the upper 
levels of the forest, 3 of h for Glossophaga and kO of 5^ for Phy 1 losto- 
mus . For P_. d i scolor preference for flying above groundstory shrubs is 
highly significant (P_<.01, Chi Square Test). 
Habi tat select ion 

Phyllostomus discolor was common in the mature forest and second 
growth but uncommon over creeks. Some of the important tree species 
producing flowers and fruits eaten by Phyl lostomus are common only in 
second growth (e.g. Ochroma ) ; others are common only in mature forest 
(e.g. Pseudobombax ) ; and still others are common in both habitats (e.g., 
Cecropia ) . 
Feed! ng behavior 

During the dry season bats are frequently captured with pollen 
heavily dusted over the anterior parts of the body. It is likely that 
these animals visit a number of flowers in succession, consuming nectar 
and performing pollination services at each flower, and then later 
perch to ingest pollen by grooming it from the fur and skin. 

None of the bats in this guild were captured carrying fruit in the 
mouth, and it is not known whether they use night feeding roosts. 

Sixty-nine percent of all P_. discolor captured in all-night samples 
were taken within two hours of sunset. Such a strong unimodal pattern 



70 
of flight activity (Fig. 9) also is reported by LaVal (1970) and suggested 
by Heithaus e_t_ aj_. (197*0 for this species in Costa Rica. My data are 
insufficient for discussing the flight activity cycle of Glossophaga ; 
however, LaVal (1970) reports a strong peak in activity at dusk and in 
the first hour of darkness just before the peak in P_. di scolor act ivi ty . 
Sanguivore Guild 
Body s ize 

Of the three extant vampire species, only Desmodus rotundus , the 
common vampire, occurs on Barro Colorado Island and in the surrounding 
vicinity. The pre-meal mean body weight of D_. rotundus is 33-5 g. 
Food sel ection 

Wild vampires feed only on the blood of homoiothermi c vertebrates 
(McNab, 1973). While vampire feeding behavior and prey selection is 
well documented in agricultural areas where domestic livestock are the 
chief food source (Turner, 1975), nothing is known of the prey species 
of vampires in remote areas where only wild animals are potential hosts. 
Vert ical, stratification 

Where domestic animals are the source of food, vampires fly almost 
exclusively within 3 m of ground level (Bonaccorso, unpublished data). 
It is possible that vampires more commonly fly in the canopy level in 
isolated forests where arboreal species (e.g., monkeys and birds) may be 
important sources of blood meals for these bats. On Barro Colorado 
Island two vampires were captured in subcanopy nets and one in a ground 
net. 
Habi tat selection 

Vampires were clearly more abundant on Buena Vista Peninsula than on 
Barro Colorado Island. Desmodus was the fourth most abundant species in 



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73 
the Buena Vista samples {1-3% of the total captures), whereas on Barro 
Colorado Desmodus was one of the least commonly captured species (0.2% 
of the total captures, and see Fig. k) . Horses, cattle, pigs, and fowl 
of the scattered farms in the Buena Vista-Fr i joles area provide a 
dependable and abundant food source that "los vampiros" constantly para- 
sitize (Fulo Sanchez, pers. comm.). 
Gleaning Carnivore Gui Id 
Body s ize 

The largest feeding guild within the bat fauna of Barro Colorado, 
the gleaning carnivore guild, is formed by nine species of phyl lostomi ne 
bats. This guild also presents the largest range in body size within 
any of the BC1 feeding guilds (Table 20). Micronycter is megaloti s, one 
of the smallest bats on Barro Colorado, has a mean body weight of 6.3 9-, 
while Vampyrum spectrum , the largest species on the island, weighs 
about 120 g. 

The increment in body weight between successively larger species is 
more irregular within the gleaning carnivore guild than in any other 
guild on the island (see Fig. 3). Two species have mean body weights 
of close 'to 15 g.> and three species have mean body weights of 31 to 
36 g. On the other hand all three species of the genus Mi cronycter is 
differ from the next smaller species by a factor of 1.5. 
Food species sel ect ion 

Little precise information can be offered at this time concerning 
the prey species eaten by members of this guild. Excepting Vampyrum 
spectrum , guild members feed predominately on insects most of the year. 
I have a large collection of fecal samples from these species but as 
yet have found no one able to identify the minutely fragmented insect 
exoskeletons that constitute these samples. 



7* 



Table 20. Weights in grams of gleaning carnivore bat species on 
Barro Colorado. 



Bat species 



Mean Standard Sample Wgt, / Wgt 
(x) Deviation size Ig sm 

(S. D.) (N) 



M. megalot is 



M. 


brachyot is 


M. 


crenulatum 


M. 


hi rsuta 


T. 


ci rrhosus 


T. 


sy 1 vi col a 


T. 

P. 


b i dens 
hastatus 


V. 


spectrum 



6.3 


0.6 


6 


-- 


9.7 


1 .1 


3 


1.53 


U.7 


0.7 


,]2 


1.52 


15.2 


1.2 


1 


1 .03 


31 .0 


3-8 


13 


2.09 


32.6 


3.6 


10 


1 .04 


35.6 


2.3 


7 


1 .09 


91 .2 


k.O 


7 


2.56 


20.0 


__ 


1 


1.31 



1-57 



" Weight of larger species divided by weight of smaller species 
in the pair compared. 



75 

On the basis of characteristics of echolocation, Novick (1970 
hypothesized that large-eared insect- and vertebrate-eating bats, such 
as are found in the gleaning carnivore guild, are adapted to distinguish 
and capture prey items resting on foliage. Ross (1 967) and Wilson (1971b) 
have shown in food habit studies that three such large-eared species, 
Antrozous pal 1 idus , Macrotus waterhousi i and Mi cronycteri s hirsuta , do 
feed primarily on large insects that spend much of their time perching 
on vegetation or on the ground. Gardner's (1975) review of the scattered 
information on food habits of the bats in this guild further confirms 
that food items such as lizards and large insects probably are gleaned 

from fol iage. 

Micronycteris . Wilson (I971 b ) reported that large roaches, Orthop- 
tera, and scarabeid beetles are the most important items in the diet of 
M. hirsuta on Orchid Island, a small island adjacent to Barro Colorado. 
During the dry season, fruit became an important component of the diet 
of this species as indicated by droppings below the study roost. My 
food samples show that M. mega lot is and M. brachyotis also switch in 
part to fruit, diets in the dry season. M. brachyotis also eats nectar 
and pollen. An individual captured in mid-December was thoroughly dusted 
ith the pollen of a balsa tree ( Ochroma lagopus ) . 

Tonatia. A very large male cicada ( Fidicina mannifera ) weighing 
2.5 g was carried into a net in the mouth of a Tonatia bidens in July 
of 197^. The prothorax of the cicada had been crushed by the bat's 
teeth and the cicada was dead when removed from the net. Because this 
event occurred in the mating season of the cicadas, amongst the loud 
nocturnal chorusing of the males, it posed the question of how Tonatia 
locates such insect prey. Do bats locate such prey items via echoloca- 
tion or sounds produced by the insects? 



w 



76 

Two T. bidens , one male and one female, were released in a large 
outdoor flight cage, one at a time, on BCI. Both individuals were 
immediately attracted to the sounds of calling male cicadas that I held 
by forceps inside the cage. The cicadas were plucked from the forceps 
by the flying bats and eaten with gusto at a perch. Female cicadas 
held so that their wings could not move in the forceps were ignored by 
these bats; however, when the wings were allowed to flap nosily, the 
bats again were attracted to the cicadas and ate them. During later 
experiments large nocturnal grasshoppers, katydids, beetles, and moths 
(species not identified) placed on the inside cage screening were 
"gleaned" from the screening and eaten by these bats. It is obvious 
that Tonatia bidens was able to locate cicadas from sounds produced by 
the cicadas, but whether other large foliage-clinging insects, many of 
which produce ultrasound, were echolocated or detected from insect- 
produced sounds remains an interesting question for future research. 

Only insect fragments were found in the fecal samples of T. bidens 
and T. sylvicola from BCI. 

Phyl lostomus . Insects and fruits were found in the fecal samples 
of Phyl lostomus hastatus . It also has been reported by several authors 
to eat birds and rodents (Gardner, 1975). 

Vampyrum . Vampyrum spectrum , the false vampire bat, is the largest 
New World bat. It appears to feed primarily on birds and small mammals, 
though investigators report some fruit and insects in its diet (Gardner, 
1975). A hollow tree roost monitored by J. Bradbury (pers. comm.) in 
Costa Rica had a steady flow of feathers from parrots, trogons, cuckoos, 
anis, and many other birds appearing at its base. D. J. Howell and I 
kept a Vampyrum al ive in captivity for three weeks on a diet of small bats 



77 
and birds ranging in size to large doves (Howell and Burch, 1974). When 
released in a large room with small fruit bats (10-20 g) the false 
vampire would fly up behind its flying victim and slap it into its jaws 
with a wingtip. One morning at sunrise on Barro Colorado, a false vam- 
pire circled about an Artibeus jamaicensis I was untangling from a net. 
The Vampyrum was apparently attracted by the alarm calls of the fruit 
bat and circled for over a minute before leaving. 

Mimon . Fecal samples of Mimon crenulatum from BCI appear to contain 
only insect chitin. 

Trachops . Fecal samples of Trachops ci rrhosus from BCI appear to 
contain only insect chitin, but this species is reported to eat lizards 
such as anoles and geckos that are gleaned from vegetation, as well as 
some fruit (Gardner 1975; Howell and Burch, 1974). 
Verti cal strati f i cation 

Mimon crenulatum and Tonatia sylvicola show a signi f icant preference 
for flight in the groundstory level of the forest ; and the small samples 
for Micronycteris brachyotis and Tonatia bidens are just barely below 
significance levels for showing a preference for flight activity in the 
subcanopy-canopy level (Table 21 ). Thus the two similarly sized species 
of Tonatia appear to forage in separate vertical strata. 

Should future research increase sample sizes on vertical stratifi- 
cation it would not surprise me if none of the three species of the 
genus Micronycteri s show a strong preference for one particular vertical 
stratum. All three species are very different in body size and probably 
specialize on mutually exclusive sizes of prey items. 

Though the data are very limited, the two very large species in this 
gui Id, Phy 1 lostomus hastatus and Vampyrum spectrum were captured or seen 



73 



Table 21. Vertical stratification of gleaning carnivore species on 
Barro Colorado. 



Sat species 



No. of bats captured No. of bats captured 
at ground level, at subcanopy levels, 
1 to 3 mm 3 to 12 mm 



M. mega lot is 



M. 


brachyot is 


M. 


hi rsuta 


M. 


crenulatum 


T. 


ci rrhosus 


T. 


syl vicol a 


T, 

P. 


b idens 
hastatus 


V. 


spectrum + 



1 

6 
6 

9- 
5 

18** 
2 





3 
12 
3 
1 
2 

3 
8 

h 
3 



- : Significant by Chi Square Test (_P_ < .05) . 

-'"- Highly significant by Chi Square Test (P <.0l). 

+ Based on two net captures in Costa Rica and one visual sighting on 
on Barro Colorado 

Yates Correction for Continuity is used on all Chi Square Tests (Sokall 
and Rohlf, 1969) . 



79 
flying only in the subcanopy-canopy levels of the forest. The ground- 
story (0 to 3 m) on Barro Colorado has the most dense foliage cover of 
any of the vertical strata of the BC1 forest (E. Leigh, unpubl . data). 
P. hastatus and V_. spectrum may be too large to maneuver well through 
the thick groundstory vegetation. 
Habi tat selection 

Several gleaning carnivore species prefer either creek or forest 
habitats on Barro Colorado to the exclusion or near exclusion of the 
other habitat. Micronycter i s brachyoti s and Tonatia sy 1 v i co 1 a are both 
common species in the forest station samples but were totally absent from 
creek samples (Fig. 6). Tracho ps cirrhosus represents k% of all individ- 
ual bats sampled at creek stations (8th most abundant species in creek 
samples) but only 0.5% of the individuals sampled at forest stations 
(17th most abundant species in forest stations). All other species in 
the guild are approximately equally abundant in creek and forest samples. 
Comparisons with Buena Vista second growth samples are not made because 
most species in this guild were under-represented at Buena Vista from lack 
of harp-trapping. 

So far I show that most bat species within a given feeding guild 
partition food resources on the basis of food particle size. However, 
some of the gleaning carnivores seem to use additional mechanisms to 
partition food resources between similarly sized species. 

The existing data make it appear that a spatial mechanism, special- 
ization in foraging microhabi tat , permits Trachops cirrhosus , Tonatia 
sylvicola , and Tonatia biden s, all similar sized gleaning carnivores, 
to partition food resources within the same macrohabi tat . i suggest 
that T. ci rrhosus specializes on prey items it can glean from low 



80 
foliage along creeks, that T. sylvicola special i zes on prey items it can 
glean from groundstory foliage in the forest, and that T\ b_i_dens_ special- 
izes on prey items it can glean from trees in the forest and along creeks 
or from the ground. Future research likely will show that all three 
species eat invertebrates and vertebrates weighing between 2 and 15 g, 
including lizards, frogs, and large insects. 
Feed ing behavior 

The gleaning carnivores eat rather large prey items relative to 
their body weight. It probably is common for them to carry prey to a 
feeding roost or day roost for consumption (Wilson, 1971b; Bradbury, 
pers . comm. ) , 

Data on activity cycles are too scant for meaningful analysis. 
M_. brachyotis , M. crenulatum , T_. sylvicola , and T. ci rrhosus appear to 
have a major peak of activity in the first two hours after sunset. 
Slow-flying Hawking Insect i vore Gui Id 

Eight species belonging to three families constitute the guild of 
slow-flying hawking insect ivores . Four species belong to the Emballonu- 
ridae, two to the Vesperti 1 ion idae, and two to the Mormoopidae. An 
additional species, Thyroptera tricolor of the Thyropter i dae, is known 
in recent years only from a single 1973 sighting on BCI. T. tricolor 
perhaps should be included in this guild if a population still exists 
on BCI, but the species is probably near extirpation on the island be- 
cause of plant succession that has resulted in the disappearance of 
most large-leafed groundstory plants (e.g. Musa and Cal 1 i thea ) used as 
roosts (Findley and Wilson, 197*0- 



81 
Body size 

Mean body weights of the species in this guild range from h.Z to 
22.6 g (Table 22). Wing morphology and flight behavior (Bonaccorso, 
unpubl. data) suggest that species within the same family are most 
similar in foraging behavior. Thus, species are grouped in subguilds 
by families. The two mormoopids differ in mean body weight by a factor 
of 1.37, a figure that suggests these two species may divide food 
resources solely on the basis of particle size. The two vespert i 1 ion ids , 
on the other hand, are very similar in body size. Analysis of the rela- 
tionships among body weights of the four embal lonur i ds is complicated by 
small sample sizes and sexual dimorphism. The mean body weights of males 
of the four species differ by a factor of 1.25 to 1.47. 
Food select ion 

All species of this guild appear to feed on fairly small flying 
insects. Prey items are eaten on the wing rather than carried to feed- 
ing roosts. Some embal lonurids hover around tree foliage and probably 
feed to some extent on insects attracted to host trees. One BC1 fecal 
sample from Pteronotus parnellii examined by Terry Erwin contained leg 
parts of a small beetle of the family Alicuidae. All other samples await 
analysis. 
Vertical stratification 

Pteronotus parnellii almost exclusively restricts its flight to 
within 3 m of the ground (Table 23) ■ Myotis nigricans and £. bilineata 
apparently fly with nearly equal frequency in groundstory and subcanopy 
levels of the forest. Peropteryx kappleri is probably a specialist on 
insects of the subcanopy, as indicated by the capture of all four BCI 
individuals in high nets and numerous visual observations made by the 
author in Belize (unpubl. data). 



82 



Table 22. Weights in grams of slow-flying hawking insectivore bat 
species on Barro Colorado. 



Bat species Mean Standard Sample Wgt / Wgt* 

vi ) deviation s ize In 

(S. D.) (N) 



— • T e Ptura ** 
_C. max i mi 1 1 ian i »* 
— ■ — ! ' ne ata males 
S. bi 1 ineata females 



Embal lonuri dae 



sm 



4.2 


— 


1 


-- 


5.2 


— 


2 


1 .25 


7.7 


0.56 


11 


1.47 


8.7 


0.7 


3 


— 


11.2 


-- 


2 


1.46 



—• kappleri ■k * 

Vespert i 1 ion idae 
— tumida 4 # 2 -- 2 

M. nigricans k.h 0.67 11 1 .05 

Mormoop i dae 
P_. suapurens is 16.5 -- 1 

P. pa me 11 i i 22.6 1.48 30 1 .37 



* Weight of larger species divided by weight of smaller species in the 
pa i r compa red. 

"- Males and females are probably dimorphic in body weight. 



83 



Table 23. Vertical stratification of slow-flying hawking insectivore species 
on Barro Colorado 



No. of bats captured at No. of bats captured at 
Bat species ground level, 1 to 3 m subcanopy levels, 3 to 1 2 m 



_S. bi 1 ineata 7 k 

_C_. maximi 1 1 iani 2 

_P. kappler i k 

R. tumida 1 

—' nigricans 3 3 

£.• parnell i i 7^*- : 1 

** Highly significant by Chi Square Test (P<.01) with Yates. 
Correction for Continuity (Sokall and Rohlf, 1 369 ) . 



84 

Hab i tat select ion 

_P. p arnel 1 i i is the second most abundant species in the forest 
station samples but is very rare in the creeks (Fig. k) . The only 
specimen of P. suapurens is was captured in the forest. 

Myotis nigricans was captured only at forest stations, whereas 
Rhogeesa tumida was captured only at or near creeks. These two 
similar-sized species may differ in habitat requirements. 

Visual observations of Saccopteryx b i 1 ineata were possible because 
this species is crepuscular. Individuals repeatedly fly in circles around 
feeding territories in small clearings of the forest (e.g. . treefal Is) or 
over creeks (J. Bradbury, pers. comm.). 1 have frequently watched territory 
holders chase intruding conspecifics out of their territories emitting high 
pitched audible sounds as they fly. 
Fl ight behavior 

Pteronotus parnel 1 i i is one of the most commonly seen species on 
Barro Colorado, as it flies low along forest trails. Ultrasonic pulses 
picked up by a bat detector indicate that _P. parnel 1 i i feeds as it flys back 
and forth in long loops along the forest trails and groundstory vegetation. 

The flight activity of P. parnel 1 i i through the course of the night is 
bimodal with a major peak of activity occurring one to four hours after sun- 
set and a minor peak occurring eight to ten hours after sunset (Fig. 10). 
Data on activity cycles of other species are limited, but £. parnel 1 J i 
appears to be the only species in the slow-flying hawking guild that has no 
strong peak of activity the first hour after sunset. Based on netting, 
visual observations, and ultrasonic detection, the embal lonur ids are active 
from an hour before sunset to an hour after sunset and again at a similar 
period about sunrise. 



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REPRODUCTION 
Three patterns of reproduction occur in Neotropical bats: seasonal 
monestry, seasonal polyestry, and year-round polyestry (Fleming, 1973). 
Present information indicates that a single young is born per litter 
except in the genus Rhogeessa in which the usual litter size is two 
(Humphrey and Bonaccorso, 1975). 
Canopy Frugivore Gui Id 

Canopy frugivores are seasonally polyestrous, with one birth peak 
at the end of the dry-to-wet transition and a second about the middle 
of the wet season (Figs. 11-13 and Table 25; Wilson, 1975) . The first 
birth peak for all species coincides with the beginning of the first 
predictably steady rains of the year in late April and May, a time of 
fruit abundance. Large species such as A. jamaicensis and A. lituratus 
are pregnant (as detectable by palpation) by the first week of January. 
Small species like A. phaeotu^ are not in a similar stage of pregnancy 
until late January. Lactation then proceeds for one or two months during 
a period of food abundance. There is a postpartum estrous,and females 
are well advanced in the second pregnancy of the year while lactation is 
still underway (Fleming, 1971). 

The second birth and lactation peaks are less synchronized among 
species because of differences in gestation and lactation periods; the 
same is true to a lesser degree within species because of individual 
variation. For example, the second peak of lactation occurs in July- 
September for A. jamalcensi^ and A. phaeotis , but not until September- 

87 



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96 
November for the larger A_. 1 i turatus . 

All canopy frugivores are reproduct i vely quiescent in the late wet 
season. Females of small species appear inactive from October through 
December. The two largest species of the guild appear reproducti vely 
inactive from mid-October through December, at least by external signs, 
but histological preparations (Fleming, 1970 indicate that A. jamaicens is 
females are in the early stages of pregnancy with drastically slowed 
embryonic growth occurring in these months. Whether other species also 
pass through a period of delayed development at the end of the wet season 
is not known. Nevertheless, the energetic budget channeled into repro- 
duction by each canopy frugivore species is markedly reduced during the 
late wet season, a time of fruit scarcity. 

During the March-May sampling, 27% of the A. j amaicensi s adult 
females captured were nulliparous (Fig. 1*0, and nearly all of these 
probably had been born in the first or second birth pulse of the previous 
year' (8 to 12 months before). Through the next three sampling periods 
the percentage of nulliparous females in the sampled population steadily 
rose to k3% as recruitment occurred from the offspring of the year. 
Between November and the following March the proportion of nulliparous 
females declined, not from their having given birth, but presumably from 
higher mortality and/or dispersal rates than are found in older females. 
Such data from other species are too few to provide comparison. 
Grounds tory Frugivore Guild 

Groundstory frugivores follow a reproductive pattern similar to 
canopy frugivores. There are two births per year per female, one in 
the dry-to-wet season transition and the other in mid-wet season (Fig. ]k). 



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99 
That females have a postpartum estrous is indicated by simultaneous 
pregnancy and lactation in March-May and recaptures of marked individ- 
uals. Females are reproducti vel y inactive from mid-October through 
December. 
Scaveng ing Frug i vore Guild 

Though only two female Centurio were captured during the study, 
one female pregnant in February and another lactating in November indi- 
cate that the wrinkle-faced bat is probably seasonally polyestrous like 
other fruit bats. 
Pol len-Nectar-Frui t- I nsect Omni vore Gu i 1 d 

The only reproductive data available from Barro Colorado are for 
Phyllostomus discolor , which appears to follow the pattern of seasonal 
polyestry explained for frugivorous guilds (Table 26). 

* 

Sanguivore Gui Id 

Though only six adult female vampires were captured during the 
study the appearance of pregnant females in June, July, and August and a 
lactating female in January suggest that Desmodus r otundus is either 
seasonal ly polyestrous or, as suggested by Wimsatt and Trapido (1952), 
polyestrous year round. 
Glean i ng Cam i vore Guild 

The fragmentary data available for this guild suggest a bimodal 
pattern of seasonal polestry for the genera M i crony cter is , Tra chops , and 
Tonat ia . The first birth pulse in these genera coincides with the begin- 
ning of the wet season (Table 26 and Wilson, 1975). A pregnant and lac- 
tating female Tonatia sylvicola captured in March provides the first 
evidence that this species has two litters per year and a postpartum 
estrous . 






100 
Mimon crenulatum has a monestrous reproductive cycle (Table 26). 
The peak in pregnancies occurs in the dry-to-wet season transition with 
lactations peaking in the early wet season. Mimon are reproduct i vely 
inactive from September through December. 
Slow-f ly i ng Hawking Insect ivore Gui Id 

Female Pteronotus parnellii are monestrous (Fig. 15). Pregnancies 
occur from late December through mid-April. Lactation proceeds from 
mid-March through late October; however, most young bats are weaned by 
mid-July. The percentage of females suckling young in the May-July 
sampling indicates that at least 53% of the adult females succeed in 
raising young to the latter stages of nursing. This latter figure is in 
reality much larger because some females have already weaned young by 
the end of this sampling period. Unfortunately juvenile P_. pa rnel 1 i i 
cannot be distinguished from adults on the basis of pelage color as is 
possible for many other species. 

•During the March-May sampling 16% of the captured females were 
nulliparpus adults, and these were probably all one-year-olds. However, 
in the next sampling period 50% of the females captured were nulliparous, 
indicating that young of the year were entering the flying population 
(top graph in Fig. 15). In the July-September sample, 65% of the females 
were nulliparous. The number of nulliparous females then declined to 
k~/% by the next sampling period; associated with the fact that only 16% 
of the females were nulliparous in March, this pattern suggests a high 
mortality for females in the latter half of their first year. Such a 
pattern has been found in temperate Myotis (Humphrey, 1975b). 



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CONCLUSIONS 

Though tropical forests are relatively stable terrestrial environ- 
ments, nearly all animal species must seasonally alter their foraging 
and reproductive behavior in response to fluctuating environments whether 
they be food general ists such as coatis (Kaufmann, 1962) and red-winged 
blackbirds (Orians, 1973) or food specialists such as three-toed sloths 
(Montgomery and Sunquist, 197^) > anteaters (Lubin and Montgomery, unpubl . 
data) and hummingbirds (Wolf, 1970; Snow and Snow, 1972). Several recent 
papers have discussed how Central American bats respond to seasonal 
changes by altering foraging and reproductive behavior (Mares and Wilson, 
1971; Fleming et_ aj_. , 1972; Hei thaus e_t_ a_l_. ; 1975; Humphrey and 
Bonaccorso, 1975). The present study shows that on Barro Colorado Island, 
Panama, bat species diversity, as well as foraging and reproductive stra- 
tegies of individual bat species, all undergo marked seasonal variation 
in the moist tropical forest. 
Species Divers i ty and Phenology 

Maximal diversity in the bat community of Barro Colorado occurs from 
March through July, the principal growing season. During this time rains 
are frequent yet mild and many plants and insects, having passed through 
reproductive inactivity in the dry season (except for flowering activity), 
undergo rapid growth and reproduction. Deciduous trees flush new leaves 
and mature fruits become abundant both in diversity and biomass. Most 
of the large orders of insects including Coleoptera, Lep i doptera, and 

103 



10*f 
Hymenoptera explosively increase in numbers of individuals and biomass. 
In general most of the food resources eaten by bats, with the exception 
of flowers, are abundant during the March-July period and many species 
of bats that move out of this forest habitat in the late wet season 
return by March. 

Minimal diversity within the bat community occurs in the late wet 
season. Fruit is scarce in both kinds of mature fruits and total biomass, 
and fruit bat species diversity is lowest during this period. The species 
diversity of insectivorous bat species also reaches a minimum during the 
late wet season, and though the actual total numbers and biomass of in- 
sects are probably slightly lower in the dry season, the availability of 
insects as food for bats is probably lowest in the late wet season, when 
frequent heavy rains often curtail insect and bat activity. 

Annual variation of physical and biotic factors in the tropical 
forest also appears to affect the diversity of the bat community. Rain- 
fall may fluctuate drastically from year to year in absolute amount and 
distribution through the year (Smythe, 197*0- An extended wet season may 
prevent or destroy flowers in a given year and a late dry season may hin- 
der or delay fruit production or insect reproduction. Furthermore some 
species of plants do not reproduce every year (Foster, 1973; Frankie 
et al . , 197*0- The diversity and abundance of bat species were somewhat 
different in magnitude each of the three years on Barro Colorado. The 
causal factors that influence annual variation in the bat community are 
unclear but probably involve predation, food supply, and competition. 

At the ordinal level, the communities formed by tropical bats are 
by far the most complex assemblages of sympatric mammalian species occur- 
ring anywhere in the world. Much simpler communities of bats are found 



105 

in temperate latitudes. For example, Panama supports ]0k known species 
of bats (Handley, 1967) , whereas similarly sized South Carolina contains 
only ]h species and the whole of the United States and Canada contains 
only 39 species (Hall and Kelson, 1959). Furthermore, 35 to 50 species of 
bats are commonly found coexisting within an area of a few square miles in 
Neotropical forests. Why are there so many more species of bats in tropi- 
cal regions than are found in temperate regions of similar size? What 
mechanisms permit so many similar species to coexist in tropical forest 
communi ties? 

Orians (1969) concluded that tropical forests . support more bird 
species than temperate forests because of two attributes unique to the 
tropics. Firstly, many kinds of food items that are ephemeral in supply 
in temperate latitudes are available year-round in tropical latitudes 
(e.g. fruits and flowers). Secondly, the structure of the vegetation in 
tropical forests is much more heterogenous than in temperate forests, thus 
providing more foraging microhabits for specialization (e.g. bromeliads 
and 1 ianas) . 

The great variety of year-round food items and habitat heterogeneity 
in tropical forests go a long way toward explaining the abundant numbers 
and kinds of bat species in the tropics. Forty-one species in Panama are 
probably fully insectivorous and the other 63 species feed on fruit, pollen 
and nectar, fish, vertebrates, blood, or some combination of the above. 
All Nearctic bats north 32° N latitude are fully insectivorous in food 
habits. Still there are three times as many insectivorous bats in Panama 
as in South Carolina. Future research may explain this as being due to a 
greater variety and size range in Panamanian insects and additional kinds 



i 



106 

of microhabitats in which to capture insects. It is notable that at 
least 10 species in Panama probably feed to some extent by gleaning 
foliage, whereas only one bat species in South Carol ina does so. A number 
of emballonurids appear to feed much of the time on aerial insects that 
are flying around foliage, flowers, or fruits. Several species feed 
chiefly on insects found over water or on its surface (Hooper and Brown, 
1968; Gardner, 1975). 
Foraging and Reproductive Strategies 
Canopy f rugi vores 

Resource £art i t ion ing_ _m the canopy frugjvore guM^. Most fruits 
preferred by bats have attributes of color, odor, taste, etc. that make 
them unavailable to or not preferred by other kinds of fruit-eating 
animals (Humphrey and Bonaccorso, 1975). Hence, most of the competitive 
interactions any bat species encounters over fruit resources, either in 
ecological or recent evolutionary time, are with other species of bats 
of its own feeding guild. The foraging strategies of fruit bats should 
optimize the intake of energy with respect to the density, abundance, 
spatial distribution, and particle sizes of available bat fruits. Addi- 
tionally/ temporal partitioning of the access to fruits may arise when 
the resource is concentrated in a small space (e.g. one large fruit tree 
with many fruits). Of course, fruits themselves do not have activity 
cycles that limit a bat's access to them, and once a fruit is mature it is 
available to any animal that would eat it. 

Moist forest sites throughout Central America usually contain eight 
to ten species of canopy frugivores. Eight species of stenodermine bats 
form the canopy frugivore guild on Barro Colorado. These bats feed almost 



107 
entirely on fruits growing in the forest canopy on trees, vines, and epi- 
phytes. Individuals of most of these plants occur at very low densities 
and in patchy distributions within the forest. Most of the resource trees 
are very large and produce enough fruit to feed hundreds of bats every 
night during their fruiting periods of a week or so. Because a great 
range in the size of preferred canopy fruits is available, it is possible 
for many bat species to specialize in taking food particles of a particular 
size class. Seven species on BCI are fig specialists that partition figs 
primarily on the basis of size. The other species is a general ist with 
regard to the types of fruit in its diet. 

The fig specialists appear to have large home ranges (about 3 km 2 
f° r Artibeu s jarna i cens i s ) compared to other bats of similar size, and 
they travel through much of the home range in the course of a night 
searching for widely scattered resource plants (Heithaus e_t _a J_. , 1375; 
Morrison, 1375; Bonaccorso, unpubl. data). Artibeus phaeotis , the fruit 
general ist, appears to have a comparatively small home range for its size, 
probably because it feeds on more kinds of fruits and thus is more likely 
to encounter a suitable food resource in a smaller area than a fruit 
speci a 1 i st . 

The foraging strategy of canop y f ru gi vores on Barro Colorad o . 
Frugivorous bats consume about their own weight in fruit per night 
because they appear to have low assimilation efficiencies and do have 
high metabolic rates (McNab, 1369). Each bat must make about a dozen 
visits to one or a few resource trees per night. Each visit involves 
picking a single fruit and carrying it away to a feeding roost where the 
fruit is ingested. Once a tree with mature fruits is located an individ- 
ual bat may return to it repeatedly for over a week, but much time and 



108 



energy are spent scouting for trees that will be in fruit in future days 
(Morrison, 1975). 

For at least a couple of weeks during the beginning of the dry season 
when fruits are scarce and bat pollinated flowers are very abundant, at 
least three of the canopy frugivores switch partly to pollen and nectar 
diets. In drier forest habitats where suitable flowers are available over 
a longer dry season, stenodermine bats feed on nectar and pollen through 
much of the dry season (Heithaus et_ aj_. , 1975) - 

The reprod uctive strategy of canopy f rugi vores o_n_ Barro Colorado. 
Adult females have two litters per year. Birth pulses are synchronized 
within populations and coincide with the two predictable seasonal peaks in 
fruit abundance. Late term pregnancy, lactation, and the learning 
processes associated with foraging by young bats, the events of highest 
energetic cost in the life cycle of these bats, occur at times of food 
abundance. The proximal cues that provide the timing for reproductive 
activities are not known but may involve rainfall or photoperiod. 
G r o u nds to r y f ru g i vores 

Resource parti tioning in the groundstory f rug i v ore guild . Ground- 
story frugivores specialize on eating fruits that grow on shrubs, most of 
which are less than 3 m in height. To a lesser extent these bats also 
feed on canopy fruits, and in dry forest areas of Belize (Bonaccorso, 
unpubl . data) and Costa Rica (Heithaus et_ aj_. , 1975) guild members also 
feed on nectar and pollen in the long dry season. 

Two species in the Carol linae, Carol 1 ia castanea and C_. perspi ci 1 lata , 
form the groundstory frugivore guild on Barro Colorado. In any one place 
in closed canopy forest habitat throughout the Neotropical region, this 



109 

guild contains fewer species than the canopy frugivore guild. In South 
America the other genus in the subfamily Carol linae, Rhinophyll a, appears 
to fit into the groundstory guild from information in Handley ( 1 g67> that 
they are captured mostly in ground level nets. Some species of the 
stenodermine genus Sturnira may also fit into the groundstory guild. 
Far fewer shrub species than tree species produce bat-dispersed 
fruits in tropical forests of Central America (12 versus 27 known species 
on BCl; and see Heithaus et ak , 1975). Also, shrubs produce a much 
smaller range of fruit sizes than do trees. On Barro Colorado shrub 
fruits preferred by bats range from about 0.2 to 2.0 g, a tenfold range; 
whereas tree fruits preferred by bats range from about 2.0 to 30 g, a 
fifteenfold range. Finally most shrub fruits are soft berries or catkins, 
but tree fruits additionally may be drupes, monkeypods, and other forms. 
Because of the greater variation in kinds, sizes, and shapes of canopy 
fruits there are many more ways to specialize on canopy fruits than on 
groundstory fruits, hence the larger numbers of species in the canopy 
frugivore gui Id. 

Ihl l£r a 9 ' 12. strategy of groundstory frugivores on Barro Colorado. 
Groundstory frugivores have small home ranges in comparison to large bats 
that specialize on canopy fruits. This probably occurs because shrub food 
species are abundant as individual plants and uniform in distribution 
compared to tree species. It is probable that a large, number of shrubs 
must be visited each night by a groundstory frugivore in order for it to 
find sufficient food. Each shrub has only a few small mature fruits 
available per night (especially true of pipers) and a given shrub may be 
stripped of fruits by other bats before an individual visits it or between 



110 



return trips from the feeding roost. When a suitable canopy species with- 
in the home range is in fruit it is included in the diet and offers a 
source of fruit for several days. Fruits are picked from the resource 
plant and carried to feeding roosts for eating. Host fruits eaten by 
these bats are mature only from one to three months consecutively; thus 
groundstory frugivores must frequently change food species and search 
images. Some insects are eaten, but it is not clear whether these are 
taken with fruits or are independently hunted. 

The reproductive strategy of the groundstory frugivores on Barro 
Colorado is essentially the same as that of canopy frugivores. 
PgJ_| en- Necta r-Fru i t- 1 nsee_t ofnnivores 

Resource partitioning _in_ the poHen-nectar-f ru i t- 1 nsect omnivore 
guild . Moist and wet tropical forests tend to have few kinds of large 
flowers suitable for bats to pollinate and use as nectar and pollen food 
resources, and these are available essentially only in the dry season 
(late December through March on BCl). Extreme nectar-pollen specialists 
among the Microchi roptera are common only in dry tropical forests and 
deserts (Humphrey and Bonaccorso, 1975). Only species like PhyUostomus 
discolor and Glossophaga soricina that switch to other types of food in 
the wet season make prolonged use of dry season flowers in moist forest, 
though some frugivores occasionally visit flowers. 

The mechanisms of resource partitioning among nectar i vorous bats 
are poorly understood. My data and those of Heithaus et aj_. (1975) and 
Alvarez and Gonzales (1970) indicate almost complete overlap among bat 
species in use of flowering plant species. Flowers do have activity 
cycles with respect to nectar product ion, and it is suggested from the 






111 

data of Heithaus et al . that temporal partitioning of floral resources is 
an important means of partitioning flowers among bats. On Barro Colorado 
the foraging activity of P_. discolor is compacted into the twilight and 
first hours of darkness, probably as a response to inter- and intraspeci- 
fic competition over nectar. The first bats that arrive at a flower each 
night receive a maximal supply of nectar and successive visitors receive 
lesser amounts (Heithaus et a 1 . , 197^)- 

The forag ing st rategy of po l 1 en -nee tar- f rui t- inse ct, omn i v ores on 
Barro Colorado . Both Glossophag a and Phy 1 los to mus appear to feed primar- 
ily on nectar and pollen as long as flowers are available. As the wet 
season begins, Phy 1 lostomus switches to fruit and insects, and Cecrop ia 
fruits become particularly important. In dry forests where Cecrop la is 
not a common tree, Phy! l ostomus disappears after the dry season flowering 
and does not reappear until the next flowering season (Heithaus et al., 
1975; Bradbury, pers. coram. )> I expect that they are migrating to and from 
habitats that have Cecrop ia fruits available in the wet season and large 
flowers .available in the dry season. 

Glossop haga too switches to fruit in the wet season, and other authors 
have found it also eating insects then (Fleming e_t_ aj . , 1972; Howell and 
Burch, 197^ ). G_. sor icina is a rare bat on BCI and becomes even rarer in 
the wet season, indicating that it may undergo habitat shifts on a seasonal 
bas is . 

The reproductive strategy of P_. discolor appears to be fairly similar 
to that of the frugivorous bats. Two birth pulses occur each year, the 
first of which is toward the end of the peak in flowering and at the begin- 
ning of the peak in fruiting. It appears that females are eating fruit 
and insects during both yearly periods of lactation. 



112 



Glean i ng earn ! vores 

Resource partitioning in gleaning carnivores . Nearly all gleaning 
carnivores depend on large insects as the primary food resource, though 
a wide range of vertebrates, invertebrates, and even fruits supplement 
the diet. This large feeding guild has a more complex array of parti- 
tioning mechanisms than any other guild on Barro Colorado. Differences 
in body size, general food types, foraging mi crohab i tats , and possibly 
activity cycles operate to maintain the ecological distinctness among 
these species. Future investigators should consider potential competi- 
tion between bats and other taxa that prey on large insects such as noc- 
turnal spiders, caprimulgid birds, and tree frogs. 

2M foraging strategy of gleaning carnivores on Ba_r ro Colo rado . 
Gleaning carnivores prey upon food items that are moderately large in 
relation to their own body weight just as fruit bats do. Also like fruit 
bats they carry individual prey items to feeding roosts whether the food 
be large insects (Wilson, 1971b) or birds (Bradbury, pers. comm. ) . Because 
of the high protein content of their diet these bats probably eat a 
smaller weight of food in proportion to their body size and also fewer 
prey items per night than do frugivores. Thus, gleaning carnivores spend 
less time and energy transporting food items between foraging sites and 
feeding roosts than do fruit bats. It would be interesting to compare 
these guilds In terms of searching effort devoted to foraging, but such 
data are not available for gleaning carnivores. 

Late in the wet season and in the dry season large insects are rela- 
tively unavailable to these bats, and some gleaning species alternate 
foraging patterns. Several of the smaller and medium sized species become 



113 

rare on the study site late in the wet season, but return and eat mixed 
diets of fruit and insects through the dry season. M,. megalotis and 
M. brachyotis appear to use this strategy. Tonatia sylvicola , however, 
remains in the BC I forest all year eating only insects. Janzen (1973) 
and Janzen and Schoener (1969) report that watersheds are dry season 
refugia for many insect groups. Perhaps some individuals or populations 
of gleaning carnivores move to riverine habitats off the island during 

lean times. 

The reprod uctive strategy of gleaning carnivores on Barro Colorado . 
Mlcronycte ris, Tonatia , and Tra chops bear two litters per year. The first 
pregnancy of the year occurs at a time of relative food scarcity, but the 
birth pulse occurs as large insects are -becoming abundant. The first 
lactation and the entire second reproductive cycle occur within months of 

food abundance. 

The peak in pregnancy for Mimon crenulatu m, a monestrous species, 
occurs about two months after those of the above gleaning carnivores. 
Thus both pregnancy and lactation occur within the year's peak of insect 
abundance. Mimon can time its reproductive activity in this manner 
because it does not squeeze two reproductive cycles within the months of 
large insect abundance as do the polyest rous species of the guild. 
Slow -flying hawki ng jnsecti vores 

Resource parti t ioning in the slow - flying hawking insect ivore gui Id . 
Much less is understood about this guild than the others discussed so 
far with respect to resource partitioning, foraging strategy, and repro- 
ductive strategy. It is possible that each family placed in this guild 
should constitute a distinct guild, but we do not know enough to be certain 



Uk 



A common denominator among all these species is that they capture small 
aerial insects and eat them while flying. All guild members probably 
have individual or group feeding territories. Territorial defense of 
foraging areas may serve as the primary means of decreasing i ntraspeci f i c 
interference over food. Body size, mi crohab i tat , and activity cycle 
differences appear to serve as the primary mechanisms that minimize Inter- 
specific competition over food within the hawking insect ivores . 

The foraging strategy of s low-flying h awking I nsectivores on Barro 
Colora do. Small insects are abundant all year long though specific kinds 
may fluctuate in abundance. These bats do not undergo major shifts in 
diet as many other guilds are forced to do. Diel foraging activity 
appears to occur in bimodal periods on a nocturnal or crepuscular regime. 
Hundreds of very small food items must be eaten each night requiring 
very high capture and feeding rates compared to other bat guilds (Gould, 
1955)- During foraging periods these bats appear to patrol the feeding 
territory constantly searching for food items via echolocat ion . 

The reproduc tive strat e gies of slow-flying hawking insectivores . 
0.' nigricans is seasonally polyestrous with reproductive inactivity during 
the heavy rains late in the wet season (Wilson, 1971a). Perhaps this is 
the only time when small insects are not abundantly available to Myotis. 
The other members of the guild appear to be monestrous. For example, 
most Pteronotus parnel 1 i i females are reproduct i ve ly active only from 
January through July, even though small insects are abundant all year 
round. Precise data on food habits and the availability of food species 
must be gathered before generalizations can be made on the reproductive 
strategies of slow-flying hawking insectivores. 



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120 



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BIOGRAPHICAL SKETCH 

Frank Joseph Bonaccorso was born 23 October 19^-8 in San Fernando, 
California. He received his Bachelor of Arts in zoology with Departments' 
Highest Honors from the University of California, at Los Angeles, in 
June 1970. In September 1970, he began work on the degree of Doctor 
of Philosophy in the Zoology Department at the University of Florida. 
In August 1975, he will begin teaching as Lecturer in the European 
Division, University College of the University of Maryland. 

Frank is a member of the American Society of Mamma logists and the 
Association for the Study of Animal Behaviour, He was awarded the 
Austin Medal by the Associates of the Florida State Museum in 1975 
for scholarly achievement and research in field biology. He also has 
distinguished himself in the art of film-making for his works -- The 
Maroon Prune K i d (1973) and The Maroon Prune Ki d Goes To Col 1 ege (1975). 



122 






i certify that I have read this study and that in my opinion it 
conforms to acceptable standards of scholarly presentation and is fully 
adequate, in scope and quality, as a dissertation for the degree of 
Doctor of Philosophy. 



A 




JC2 



John H. Kaufmann, Chairman 
Professor of Zoology 



I certify that 1 have read this study and that in my opinion it 
conforms to acceptable standards of scholarly presentation and is fully 
adequate, in scope and quality, as a dissertation for the degree of 
Doctor of Philosophy, 



■""3' /> /") / ' 7 



,/ 






Stephen R. Humphrey, Co-Chairman 
Assistant Curator in Mammalogy 
and Assistant Professor of Zoology 



I certify that I have read this study and that in my opinion it 
conforms to acceptable standards of scholarly presentation and is fully 
adequate, in scope and quality, 
Doctor of Philosophy. 



is a dissertation for the degree oF 



%?W 




Thomas C, Emmel 

Associate Professor of Zoology 



1 certify that i have read this study and that in my opinion it 
conforms to acceptable standards of scholarly presentation and is fully 
adequate, in scope and quality, as a dissertation for the degree of 
Doctor of Philosophy. 



vt£^ 




David H. H i rth 

Assistant Professor of Forestry 



I certify that I have read this study and that in my opinion it 
conforms to acceptable standards of scholarly presentation and is fully 
adequate, in scope and quality, as a dissertation for the degree of 
Doctor of Philosophy. 




Brian K. McNab 
S. Professor of Zoology 

This dissertation was submitted to the Department of Zoology in the 
College of Arts and Sciences and to the Graduate Council, and was accepted as 
partial fulfillment of the requirements for the degree of Doctor of 
Ph i losophy. 



August, 1975 



Dean, Graduate School